The biology of habitat dominance; can microbes behave as ... · Minireview The biology of habitat dominance; can microbes behave as weeds? Jonathan A. Cray, Andrew N. W. Bell, Prashanth

The biology of habitat dominance; can microbes behave as weeds?

Cray, J. A., Bell, A. N. W., Bhaganna, P., Mswaka, A. Y., Timson, D. J., & Hallsworth, J. E. (2013). The biologyof habitat dominance; can microbes behave as weeds? Microbial Biotechnology, 6(5), 453-492.https://doi.org/10.1111/1751-7915.12027

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The biology of habitat dominance; can microbesbehave as weeds?

Jonathan A. Cray, Andrew N. W. Bell, PrashanthBhaganna, Allen Y. Mswaka, David J. Timson andJohn E. Hallsworth*School of Biological Sciences, MBC, Queen’s UniversityBelfast, Belfast, BT9 7BL, Northern Ireland, UK.

Summary

Competition between microbial species is a productof, yet can lead to a reduction in, the microbial diver-sity of specific habitats. Microbial habitats can resem-ble ecological battlefields where microbial cellsstruggle to dominate and/or annihilate each other andwe explore the hypothesis that (like plant weeds)some microbes are genetically hard-wired to behavein a vigorous and ecologically aggressive manner.These ‘microbial weeds’ are able to dominate thecommunities that develop in fertile but uncolonized –or at least partially vacant – habitats via traits ena-bling them to out-grow competitors; robust toler-ances to habitat-relevant stress parameters andhighly efficient energy-generation systems; avoid-ance of or resistance to viral infection, predation andgrazers; potent antimicrobial systems; and excep-tional abilities to sequester and store resources. Inaddition, those associated with nutritionally complexhabitats are extraordinarily versatile in their utiliza-tion of diverse substrates. Weed species typically

deploy multiple types of antimicrobial includingtoxins; volatile organic compounds that act as eitherhydrophobic or highly chaotropic stressors; biosur-factants; organic acids; and moderately chaotropicsolutes that are produced in bulk quantities (e.g.acetone, ethanol). Whereas ability to dominate com-munities is habitat-specific we suggest that somemicrobial species are archetypal weeds includinggeneralists such as: Pichia anomala, Acinetobacterspp. and Pseudomonas putida; specialists such asDunaliella salina, Saccharomyces cerevisiae, Lacto-bacillus spp. and other lactic acid bacteria; freshwa-ter autotrophs Gonyostomum semen and Microcystisaeruginosa; obligate anaerobes such as Clostridiumacetobutylicum; facultative pathogens such as Rho-dotorula mucilaginosa, Pantoea ananatis and Pseu-domonas aeruginosa; and other extremotolerant andextremophilic microbes such as Aspergillus spp.,Salinibacter ruber and Haloquadratum walsbyi. Somemicrobes, such as Escherichia coli, Mycobacteriumsmegmatis and Pseudoxylaria spp., exhibit character-istics of both weed and non-weed species. Wepropose that the concept of nonweeds represents a‘dustbin’ group that includes species such as Syno-dropsis spp., Polypaecilum pisce, Metschnikowia ori-entalis, Salmonella spp., and Caulobacter crescentus.We show that microbial weeds are conceptually dis-tinct from plant weeds, microbial copiotrophs,r-strategists, and other ecophysiological groups ofmicroorganism. Microbial weed species are unlikelyto emerge from stationary-phase or other types ofclosed communities; it is open habitats that select forweed phenotypes. Specific characteristics that arecommon to diverse types of open habitat are identi-fied, and implications of weed biology and open-habitat ecology are discussed in the context of furtherstudies needed in the fields of environmental andapplied microbiology.

Introduction

As the collective metabolism and ecological activities ofmicroorganisms determine the health and sustainabilityof life on Earth it is essential to understand the function of

Received 11 October, 2012; accepted 3 December, 2012. *For cor-respondence. E-mail [email protected]; Tel. +44 (0)28 90972314 (direct line); Fax +44 (0)28 9097 5877.Microbial Biotechnology (2013) 6(5), 453–492doi:10.1111/1751-7915.12027Funding Information Funding was received from the Department ofAgriculture and Rural Development (Northern Ireland), the researchprogramme of the Kluyver Centre for Genomics of Industrial Fermen-tation which is part of the Netherlands Genomics Initiative/Netherlands Organization for Scientific Research, Biotechnology andBiological Sciences Research Council (BBSRC) for a DaphneJackson Fellowship, BBSRC and Natural Environment ResearchCouncil United Kingdom projects BBF0034711 and NE/E016804/1(respectively), and the Beaufort Marine Research Award for MarineBiodiscovery which is carried out under the Sea Change Strategy andthe Strategy for Science Technology and Innovation (2006–2013),with the support of the Marine Institute, Ireland, and J.E.H. received aProf. B. D. Tilak Fellowship from Institute of Chemical Technology-Mumbai, India.

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both individual microbes and in their communities. Thecellular systems of an insignificant portion of microbialspecies have been intensively characterized at the levelsof biochemistry, cell biology, genomics and systemsbiology; and a substantial body of (top-down) studies hasbeen published in the field of microbial ecology in relationto species interactions, community succession and envi-ronmental metagenomics. There are, however, somefundamental questions that remain unanswered in rela-tion to the behaviour of microbial species within commu-nities: what type of biology, for instance, enables microbesto dominate entire communities and their habitats andthereby determine levels of biodiversity in specificenvironments?

Plant species that primarily inhabit freshly disturbedhabitats – known as weeds – are characterized by vig-orous growth; tolerance to multiple stresses; exceptionalreproduction, dispersal and survival mechanisms; a lackof specific environmental requirements; production ofphytotoxic chemicals; and/or other competitive strategies(Table 1). The biology of plant weeds, including theirphenotypic and genetic traits, has been the subject ofextensive study over the past 100 years and is now rela-tively well characterized (Table 1; Long, 1932; Anderson,1952; Salisbury, 1961; Hill, 1977; Mack et al., 2000;Schnitzler and Bailey, 2008; Bakker et al., 2009; Chou,2010; Wu et al., 2011; Liberman et al., 2012). Wehypothesize that weed biology is also pertinent to micro-bial species, but that the defining characteristic of micro-bial weeds is their ability to dominate their respectivecommunities. In the field of plant ecology it is open habi-tats (such as freshly exposed fertile soil) that facilitatethe emergence of weed species both within specific eco-systems and across evolutionary timescales. Wepropose that weed behaviour is equally prevalent insome microbial habitats, that open microbial habitatspromote the emergence of microbial weed species, andthat microbial weed biology represents a potent ecologi-cal and evolutionary mechanism of change for somemicrobial species and their communities.

This article focuses on the following questions: (i) whattypes of substrate or environment facilitate the emer-gence of dominant microbial species, (ii) are there arche-typal weed species that can consistently dominatemicrobial communities, (iii) what are the stress biology,nutritional strategies, energy-generating capabilities,antimicrobial activities and other competitive strategies ofmicrobial weeds, (iv) which components and character-istics of microbial cells form the mechanics of weedbiology, (v) what are the properties of open (microbial)habitats that promote the emergence of weed species,and (vi) how are microbial weeds conceptually distinctfrom plant weeds, and other ecophysiological groups ofmicroorganism?

Dominance within microbial communities

The microbial diversity of specific habitats, as well as thatof Earth’s entire biosphere, is an area of intensive scien-tific interest that has implications within the fundamentalsciences and for drug discovery, biotechnology and envi-ronmental sustainability. Biodiversity provides the materialbasis for competition between microbial taxa, speciessuccession in communities, and other aspects of micro-bial ecology that collectively impact the evolution of micro-bial species (Cordero et al., 2012). We believe that certainmicrobes are genetically, and thus, metabolically hard-wired to dominate communities (monopolizing availableresources and space) and thereby reduce biodiversitywithin the habitat. Microbial communities can reach astationary-phase or climax condition with a relatively bal-anced species composition (McArthur, 2006). Howeverwhether tens or thousands of microbial species are ini-tially present (Newton et al., 2006) the community canbecome dominated by a single – or two to three – species(Fig. 1; Table S1; Randazzo et al., 2010; Cabrol et al.,2012). For example the indigenous microflora of olives iscomprised of significant quantities of phylogeneticallydiverse species such as Aureobasidium pullulans,Candida spp., Debaryomyces hansenii, Metschnikowiapulcherrima, Pichia guilliermondii, Pichia manshurica,Rhodotorula mucilaginosa and Zygowilliopsis californica(Fig. 1Bi; Nisiotou et al., 2010). Nisiotou and colleagues(2010) found that species succession and the stationary-phase community during olive fermentations are deter-mined by one dominating genus, Pichia, three species ofwhich account for almost 100% of the community by 35days (see Fig. 1Biii). The most prevalent of these, Pichiaanomala, is a microbial generalist that is not only able toinhabit ecologically and nutritionally distinct environments(e.g. palm sugar, cereals, silage, oil-contaminated soils,insects, skin, various marine habitats; see Walker, 2011)but can also dominate the communities that develop indiverse habitat types (Table S1; Tamang, 2010; Walker,2011). Studies of Pecorino Crotonese cheese fermenta-tions reveal that, even though the curd contains > 300bacterial strains, the community is eventually dominatedby Lactobacillus rhamnosus (Randazzo et al., 2010).

Species that are able to dominate communities thatdevelop in open habitats are not restricted to copiotrophs,generalists or any established ecophysiological groupingof microorganism (Table S1). Furthermore dominatingspecies span the Kingdoms of life and, collectively, can beobserved in most segments of the biosphere; from bio-aerosols to solar salterns, oceans and freshwater to sedi-ments and soils, the phyllosphere and rhizosphere, tothose with molar concentrations of salts or sugars (seeTable S1). The phenomenon can also be observed duringfood-production, food-spoilage and waste-decomposition

454 J. A. Cray et al.

© 2013 The Authors. Microbial Biotechnology published by John Wiley & Sons Ltd and Society for Applied Microbiology, MicrobialBiotechnology, 6, 453–492

Table 1. A comparison of plant weeds and microbial weeds.a

Plant weeds Microbial weedsReferences (plants/microbes)

Definition Plant species that primarilygrow in open (plant)habitatsb

Microbial species able to dominatecommunities that develop in open(microbial) habitatsc

Baker, 1965; Hill, 1977/current article; Corderoet al., 2012

Ability to rapidly occupyavailable space

Important trait Essential trait Hill, 1977/current article

Overall vigourd andcompetitive ability

Typically vigorous;competitive ability usuallysuperior to that of cropplants

Exceptional vigour and competitiveability

Hill, 1977/Figs 1 and 2;Tables S1 and 2–5

Primary competitors Intra-specific competition canbe stronger thaninter-specific competition

Intra- and inter-specific competition arelikely to be stronger if dominanceresults from efficient resourceacquisition or antimicrobialsubstances respectively

Hill, 1977/current article

Resource acquisition andstorage

Acquisition and/or storage ofwater, light, nutrients etc.typically excellent

Acquisition and/or storage of nutrients,water and/or light typically excellent

Hill, 1977; Oatham, 1997;Sadeghi et al., 2007/Table 5

Reproduction and dispersal Exceptionale May not differ from non-weed species Hill, 1977/current articleObligatory associations or

interactions with otherorganisms

Uncommon/atypical Uncommon/atypical Hill, 1977/current article

Ubiquity Many species areenvironmentally ubiquitous

Not necessarily widespread outsidethe habitat which they dominate


Germination No special requirements; hightolerance to diversestresses (see below)

No special requirements; hightolerance to diverse stresses (seebelow)


Longevity of dormantpropagules

Exceptional May not differ from non-weeds Hill, 1977/current article

Able to regenerate fromfragments

Yes, especially root fragments Not relevant Hill, 1977/current article

Maintenance of growth rateduring nutrient limitation

Some species, e.g.black-grass (Alopecurusmysuroides) onlow-potassium soils

Many (photosynthetic as well as someheterotrophic) species

Hill, 1977/Table 5; Benning,1998

Capable of creating azone-of-inhibition

Not known Yes, in some instances [Not known]/Fleming, 1929

Secretion of toxicsubstances

Some species producephytotoxic inhibitors(exuded from leaves, roots,and/or necromass)

All species produce antimicrobialtoxins (secreted into the extracellularenvironment)f

Chou, 2010/Table 6

Production of volatileorganic compounds(VOCs) that act asstressors

Some hydrophobic and highlychaotropic compounds actas phytotoxic stressors(e.g. b-caryophellene)

Many species produce a spectrum ofVOCs that can inhibit metabolicactivity at concentrations in thenanomolar or low millimolar rangef

Wang et al., 2010; Inderjitet al., 2011; Tsubo et al.,2012/Table 6

Secretion of biosurfactantsthat act as stressors

Not known Some species produce biosurfactants;substances that can solubilizehydrophobic substrates and act ascellular stressorsf

[Not known]/Tables 3 and 5;Nitschke et al., 2011

Bulk production, andsecretion, of moderatelychaotropic substances

Not known Some species produce ethanol,butanol, acetone etc. that are potentcellular stressors at millimolar andmolar concentrationsf

[Not known]/Table 6

Saprotrophic activityresulting in toxic/stressfulbreakdown products

Not known Some species degrademacromolecules to release inhibitorycatabolic products (e.g. chaotropicstressors such as phenol, catecholand vanilling)

[Not known]/Park et al.,2004; 2007; Zuroff andCurtis, 2012

Acidification of habitat Not known Some species, via bulk production oforganic acidsf

[Not known]/Table 6

Secretion of aggressiveenzymes

Unlikely Some speciesf [Not known]/Table 6; Walker,2011

Tolerance to environmentalstressesh

Tolerant to multiple, habitat-relevant stress parameters

Tolerant to multiple, habitat-relevantstress parameters

Hill, 1977/Fig. 2,Tables 2–4 and 6

Resistance to toxins and/orstressors of biotic originh

Likely Yes, most species Hill, 1977/Fig. 2;Tables 2–4 and 6

The biology of habitat dominance 455


processes where resource-rich habitats are available forcolonization (see Table S1). The materials present in andthe microbes living on these substrates are ultimatelyderived from the natural environment so community suc-cessions resulting in single-species dominance are likelyto be commonplace in comparable open habitats within

natural ecosystems (Table S1; Senthilkumar et al., 1993;Nisiotou et al., 2007; Reynisson et al., 2009; Rajala et al.,2011). Microbial weed species are able to dominate openhabitats that progress to a closed condition (e.g. ferment-ing fruit juice) as well as those that remain in a more orless perpetually open state (e.g. the surface-fluid film of

Table 1. cont.

Plant weeds Microbial weedsReferences (plants/microbes)

Phenotypic plasticity andintra-specific variation

Greater than that of cropplants

Likely to be above average (e.g. inrelation to stress biology)

Hill, 1977/current article;see references in Toddet al., 2004

Resistance to viruses,predators, and/orgrazers

Some species can tolerate,resist, and/or repel viruses,sucking insects and grazinganimals; and may containpoisonous substances – orhave morphologicaladaptations such as spines– that minimize lossesthrough grazing

Some strains/species can tolerate,resist, repel and/or avoid viruses,grazing plankton and arthropods etc;may contain toxic metabolites orhave behavioural adaptations – e.g.formation of large microcolonies –that minimize losses throughgrazing/predation; and may inhabitenvironments that are too extremefor predatory species

Thurston et al., 2001;Ralphs, 2002;Shukurov et al., 2012/Table 6

Karyotype Commonly of hybrid origin,polyploid or aneuploid

Frequency of hybrid origin, polyploidyand aneuploidy not yet tested; maycontain plasmids that contribute toweediness

Anderson, 1952/Tables 3and 5

Proportion of total species Minute (several hundredspecies)

Not yet established (likely to beminute)


Association with humanactivity

Evolution and ecology havebeen strongly favoured byland disturbance thatcreates and open (plant)habitatsi

Evolution is likely to have occurredprimarily in nature; but habitatdominance is commonplace in bothnatural and manmade environments

Anderson, 1952;Hill, 1977/Fig. 2;Tables S1 and 7

Problematic for humanendeavours

Yes, due to loss of crop-plant yieldsj; toxicity/harmto livestock; role as hostsfor crop pests anddiseases, etc.

Yes, due to spoilage of foods, drinks;some species are pathogens of cropplants, livestock or humans; mayemerge to take over industrialfermentations and other processesk

Hill, 1977/Table S1

Value to humankind Disproportionately important(origin of many crop-plantspecies; plant weeds havefood value for humans orlivestock; model organismsfor research)

Disproportionately important (keysources of bulk chemicals andantimicrobialsl; for food and drinksproduction, and otherbiotechnological applications)

Hill, 1977; Koornneefand Meinke, 2010/Table S1; seeConcluding remarks

a. Typical traits.b. Plant weeds may not be the dominating plant species.c. Not necessarily the primary habitat of the microbial weed species.d. Vigour can result from a combination of traits such as fast growth, stress tolerance, and immunity to toxins and diseases (see Tables 2–6).e. Plant weeds typically have a high output of seeds under both favourable and poor growth-conditions, and can produce seed early (prior tomaturity of the parent plant; Hill, 1977).f. Each microbial weed species may secrete diverse antimicrobial substances which can be the primary factor in habitat dominance (see Table 7;Hallsworth, 1998; Walker, 2011). For examples of the concentrations at which moderately chaotropic stressors, potent chaotropes and hydrophobicstressors can inhibit cellular systems see Bhaganna and colleagues (2010). Toxins such as antibiotics, and VOCs, biosurfactants, and otherstressors can have additional key roles in the cellular biology and ecology of microbes.g. See Hallsworth and colleagues (2003a); Bhaganna and colleagues (2010).h. Some stressors of biotic origin are structurally identical to and/or exert the same stress mechanisms as stressors of abiotic origin (e.g. seeFig. 2; Tables 2–4 and 6).i. Agricultural practices and crop-plant life-cycle can also select for early seed production and other weed traits (Hill, 1977).j. Crop-yield losses caused by plant weeds are equivalent to those caused by plant pests or plant diseases (Cramer, 1967).k. Open (microbial) habitats are not only the starting point for food and drinks fermentations, but many foodstuffs themselves represent openhabitats and it is frequently microbial weed species that cause spoilage and therefore determine shelf-life. Open habitats located on and within hostorganisms can be readily invaded by microbial weed species including those with pathogenic activities (Cerdeño-Tárraga, et al., 2005). This hasgiven rise to the use of probiotics (Molly et al., 1996; Bron et al., 2012) and a practice of preserving the skin microflora in babies and infants byavoiding use of soaps or detergents (Capone et al., 2011).l. Antimicrobial substances are used for various applications; as biofuels, biocides, pharmaceuticals, flavour compounds, food preservatives, etc.



sphagnum moss and rhizosphere of plants growing inmoist soils); see Table S1. Weeds emerge in habitatswhere competing cells are in close proximity (such asbiofilms; Table S1; Rao et al., 2005) as well as thosewhere there is limited mechanical contact between cells,such as the aqueous habitats of planktonic species(Table S1; Collado-Fabbri et al., 2011; Trigal et al., 2011;Leão et al., 2012); and in both extreme and non-extremeenvironments (Table S1). Some microbes emerge asa/the dominating species in diverse types of habitatincluding specialists such as Lactobacillus (that do so, inpart, by acidifying their environment) and generalistssuch as Aspergillus, Pichia and Pseudomonas species(Table S1; Steinkraus, 1983; Tamang, 2010). For weedspecies such as Saccharomyces cerevisiae (high-sugarenvironments), Haloquadratum walsbyi (aerobic, hyper-saline brines), and Gonyostomum semen and Microcystis

aeruginosa (eutrophic freshwater) ability to dominate canbe restricted to a specific type of habitat. Most of thesemicrobes do not populate their respective habitat as aone-off or chance event; they can consistently dominatetheir microbial communities and do so regardless oftheir initial cell number (Table S1; for P. anomala seeFig. 1; for S. cerevisiae see Pretorius, 2000; Renouf et al.,2005; Raspor et al., 2006; for L. rhamnosus see Ran-dazzo et al., 2010). It is therefore intriguing to considerwhat combination(s) of traits can give rise to a weedphenotype.

Cellular biology of microbial weeds

Stress tolerance and energy generation

During habitat colonization, even in apparently stable,homogenous environments such as sugar-based

A

B

C

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ii iii

Fer

men

tati

on

med

ium

D

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Aureobasidium pullalans Pichia guilliermondiiCandida aaseri Pichia kluyveriCandida boidinii Pichia manshuricaCandida silvae Pichia membranifaciensCandida spp. Rhodotorula diobovatumCystofilobasidium capitatum Rhodotorula mucilaginosaDebaryomyces hansenii Saccharomyces cerevisiaeMetschnikowia pulcherrima Zygowilliopsis californicaPichia anomala

Fig. 1. Percentage species compositionduring olive fermentations at (i) 2 days, (ii) 17days and (iii) 35 days over a range of condi-tions: (A) with added NaCl (6% w/v); (B)added NaCl and glucose (6% and 0.5% w/vrespectively); (C) added NaCl and lactic acid(6% w/v and 0.2% v/v respectively); and (D)NaCl, glucose and lactic acid (6% and 0.5%w/v, and 0.2% v/v respectively). Data (fromNisiotou et al., 2010) were obtained byDGGE.



solutions, there are dynamic/drastic changes in stressorconcentrations, antimicrobials and stress parameters(D’Amore et al., 1990; Hallsworth, 1998; Eshkol et al.,2009; Fialho et al., 2011; see also below). As a result ofthese fluctuations microbes are exposed to multiplestresses some of which present potentially lethal chal-lenges to the cell. In soil and sediments, for example thewater activit can oscillate from low to high and high to low;these substrates typically cycle between desiccation andrehydration and are subjected to changes in solar radia-tion, temperature, and even freezing and thawing. Soilsand sediments can be physically heterogeneous such thatwater availability, solute concentrations and other stressparameters exhibit profound spatial fluctuations. In addi-tion, intracellular metabolites and extracellular sub-stances (of both biotic and abiotic origin) impose stressesdue to ionic, osmotic, chaotropic, hydrophobic and otheractivities of solutes (see Brown, 1990; Hallsworth et al.,2003a; 2007; Lo Nostro et al., 2005; Bhaganna et al.,2010; Chin et al., 2010). On the one hand resilience tostress undoubtedly contributes to competitive ability buton the other a vigorous growth phenotype and reinforcedstress biology also require extraordinary levels of energygeneration. Furthermore, microbes that can achieve agreater net gain in energy than competing species willhave an ecological advantage (Pfeiffer et al., 2001). Herewe suggest that species able to dominate microbial com-munities are exceptionally well equipped to resist theeffects of multiple stress parameters, and that many havehigh-efficiency energy-generation systems.

We tested the hypothesis that microbial weeds areexceptionally tolerant to habitat-relevant stresses for twospecies; the soil bacterium Pseudomonas putida (Table 2)and the specialist yeast S. cerevisiae (see below). Envi-ronments in which P. putida is a major ecological player(Table S1) typically contain an array of chemically diversearomatics and hydrocarbons that induce chaotropicity-mediated stresses (Hallsworth et al., 2003a; Bhagannaet al., 2010; Cray et al., 2013). This bacterium is not onlyrenowned for its metabolic versatility, but is also known forits tolerance to specific solutes and solvents (Hallsworthet al., 2003a; Domínguez-Cuevas et al., 2006; Bhagannaet al., 2010). We compared the biotic windows for growthof P. putida for eight mechanistically distinct classes ofstress using 37 habitat-relevant substances (Table 2).This bacterium was able to tolerate all substances withineach group of stressor; this is the first data set to demon-strate that a mesophilic bacterium can tolerate the follow-ing combination of stresses: up to 4–11 mM hexane,toluene and benzene; 8–115 mM concentrations of aro-matic, chaotropic solutes; 300–825 mM chaotropic salts;1300–2160 mM sugars or polyols; 200–750 mM kosmo-tropic salts; and considerable levels of matric stress(Brown, 1990) generated by kosmotropic polysaccharides

(Table 2). The P. putida tolerance limits to highly chao-tropic substances and hydrophobic compounds weresuperior to those of other microbes (including extremo-philes and polyextremophiles; Table 2; Hallsworth et al.,2007; Bhaganna et al., 2010). Whereas prokaryotes aregenerally less tolerant to solute stress than eukaryotes(Brown, 1990), the resilience to this array of mechanisti-cally diverse solute stresses (Table 2) has neither beenequalled nor been surpassed by any microbial species toour knowledge.

Pseudomonas putida is able to avoid contact with orprevent accumulation of stressors by using solvent-effluxpumps and synthesizing extracellular polymeric sub-stances to form a protective barrier (Table 3). Thisbacterium also utilizes highly efficient macromolecule-protection systems that are upregulated in response tomultiple environmental stresses including between 10and 20 protein-stabilization proteins, oxidative-stressresponses, and upregulation of energy generation andoverall protein synthesis (Table 3). Furthermore, P. putidacan synthesize an array of compatible solutes includingbetaine, proline, N-acetylglutaminylglutamine amide, glyc-erol, mannitol and trehalose (Table 3). Individual com-patible solutes are unique in their physicochemical prop-erties, interactions with macromolecular systems andfunctional efficacy for specific roles within the cell (e.g.see Chirife et al., 1984; Crowe et al., 1984; Brown, 1990;Hallsworth and Magan, 1994a; 1995; Yancey, 2005; Bha-ganna et al., 2010; Bell et al., 2013). Microbes that areable to selectively utilize/deploy any substance(s) from arange of diverse compatible solutes have enhanced tol-erance to diverse stresses (e.g. Hallsworth and Magan,1995; Bhaganna et al., 2010). The range of compatiblesolutes utilized by P. putida may be unique for a bacterium(see Brown, 1990) and can confer tolerance to diversestresses including those imposed by chaotropes andhydrocarbons (Bhaganna et al., 2010).

The exceptionally wide growth-windows of Aspergillusspecies in relation to a number of stress parameterscorrelate with their ability to dominate communities inboth extreme and non-extreme (but physicochemicallydynamic) environments including soils, plant necromass,saline and very high-sugar habitats (Table S1). At least 20species of Aspergillus and the closely related genus Euro-tium are xerotolerant (Pitt, 1975; Brown, 1990). Aspergil-lus penicillioides is capable of hyphal growth and conidialgermination down to water activities of 0.647 and 0.68respectively (Pitt and Hocking, 1977; Williams andHallsworth, 2009); Aspergillus echinulatus can germinatedown to 0.62 (Snow, 1949). Halotolerant species such asAspergillus wentii can grow on the highly chaotropic saltguanidine-HCl at a higher concentration than any othermicrobe; up to 930 mM (≡ 26.5 kJ g-1 chaotropic activity;Hallsworth et al., 2007) and, along with Aspergillus



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.,20

10)

Phe

nolh

9.0

13.0

o-cr

esol

f3.

828.

10B

enzy

lalc

ohol

h20

.032

.7S

odiu

mbe

nzoa

tef

69.2

115

Cha

otro

pic

salts

CaC

l 2f

210

302

Cha

otro

pic

salts

occu

rin

soils

,se

dim

ents

,ev

apor

itede

posi

ts,

the

Dea

dS

ea,

brin

ela

kes

(incl

udin

gth

eD

isco

very

Bas

inlo

cate

dbe

neat

hth

eM

edite

rran

ean

Sea

and

the

Don

Juan

Pon

din

the

Ant

arct

ic)

and

mar

ine-

asso

ciat

edha

bita

tsin

clud

ing

bitte

rns

(see

Tabl

eS

1);

can

behi

ghly

stre

ssfu

lfor

,an

dle

thal

to,

mic

robi

alsy

stem

s(H

alls

wor

thet

al.,

2003

a;20

07;

Dud

aet

al.,

2004

)

MgC

l 2d

182

311

Gua

nidi

ne-H

Clh

125

640

LiC

lh59

582

5i

Alc

ohol

san

dam

ides

(mod

erat

ely

chao

trop

ic)

But

anol

d15

820

8A

lcoh

ols

are

prod

uced

byso

me

spec

ies

asan

timic

robi

als

(Tab

le6)

;et

hano

lis

used

asa

bioc

ide

and

can

occu

ras

anan

thro

poge

nic

pollu

tant

.U

rea

may

bepr

oduc

edas

anan

timic

robi

alby

som

eba

cter

ia(T

able

6)an

dis

used

asan

agric

ultu

ralf

ertil

izer

tow

hich

soil

bact

eria

are

expo

sed

Eth

anol

h60

099

3i

Ure

ah65

095

0F

orm

amid

ed16

810

80i

Rel

ativ

ely

neut

ral

subs

tanc

esM

etha

nold

970

1440

Som

eor

gani

cco

mpo

unds

have

little

chao

-or

kosm

otro

pic

activ

ityat

biol

ogic

ally

rele

vant

conc

entr

atio

ns.A

tlo

wco

ncen

trat

ions

glyc

erol

isre

lativ

ely

neut

ralb

ut,

desp

iteits

role

asa

stre

sspr

otec

tant

,ca

nac

tas

ach

aotr

opic

stre

ssor

atm

olar

conc

entr

atio

ns(W

illia

ms

and

Hal

lsw

orth

,20

09)

Eth

ylen

egl

ycol

h13

0021

60i

Glu

cose

f84

014

00G

lyce

rolf

770

2120

i

Mal

tose

f32

613

00K

osm

otro

pic

com

patib

leso

lute

s

Pro

linef

800

2000

The

maj

ority

ofm

icro

bial

com

patib

leso

lute

sar

eko

smot

ropi

cj ,in

clud

ing

othe

rco

mpa

tible

solu

tes

foun

din

P.pu

tida

and

othe

rba

cter

iasu

chas

man

nito

l,be

tain

ean

dec

toin

e.P

seud

omon

asm

ayal

soco

me

into

cont

act

with

som

eof

thes

eco

mpo

unds

via

expo

sure

topl

ant

exud

ates

Sor

bito

lf50

312

00D

imet

hyls

ulfo

xide

f35

313

00Tr

ehal

osef

474

771

Gly

cine

f99

370

Bet

aine

f15

7025

60K

osm

otro

pic

salts

NaC

lf65

075

0N

aCli

sen

viro

nmen

tally

ubiq

uito

us,

and

isth

edo

min

ant

salt

inm

ost

mar

ine

habi

tats

incl

udin

gbi

oaer

osol

s(T

able

S1)

;am

mon

ium

sulfa

tean

dK

H2P

O4

are

com

mon

lyap

plie

dto

soils

asfe

rtili

zers

.In

man

yha

bita

tsko

smot

ropi

csa

ltsar

eth

epr

imar

yos

mot

icst

ress

ors,

but

stre

sses

impo

sed

onth

ece

llar

ede

term

ined

byth

ene

tco

mbi

natio

nof

solu

teac

tiviti

esof

ions

and

othe

rsu

bsta

nces

pres

ent

(see

Hal

lsw

orth

etal

.,20

07)

KH

2PO

4f11

820

0A

mm

oniu

msu

lfate

f19

835

0S

odiu

mci

trat

ef53

500

Pol

ysac

char

ides

(kos

mot

ropi

c)D

extr

an40

000f

1017

Pse

udom

onas

putid

ais

expo

sed

toth

eko

smot

ropi

cac

tiviti

esof

and/

orm

atric

stre

ssin

duce

dby

poly

sacc

harid

essu

chas

mic

robe

-an

dpl

ant-

deriv

edex

trac

ellu

lar

poly

mer

icsu

bsta

nces

,hu

mic

subs

tanc

es,

etc.

Pol

yeth

ylen

egl

ycol

3350

f43

120

Pol

yeth

ylen

egl

ycol

6000

f20

40

a.P

ertin

entt

oth

eph

yllo

sphe

re,r

hizo

sphe

re,h

ydro

carb

on-p

ollu

ted

envi

ronm

ents

,and

othe

rhab

itats

(see

Tabl

eS

1),i

nclu

ding

cata

bolic

prod

ucts

ofhy

droc

arbo

nde

grad

atio

n,an

timic

robi

alsu

bsta

nces

(see

Tabl

e6)

,com

patib

leso

lute

s,an

dot

her

P.pu

tida

met

abol

ites.

At

suffi

cien

tco

ncen

trat

ions

solu

tes

such

asgl

ucos

e,m

alto

se,

prol

ine,

sorb

itiol

,gl

ycin

e,be

tain

e,N

aCla

ndK

H2P

O4

indu

ceos

mot

icst

ress

;w

here

asde

xtra

nan

dhi

ghM

rpo

lyet

hyle

negl

ycol

sin

duce

mat

ricst

ress

(see

Bro

wn,

1990

);hy

drop

hobi

csu

bsta

nces

typi

cally

indu

cea

(cha

otro

pici

ty-m

edia

ted)

hydr

ocar

bon-

indu

ced

wat

erst

ress

(Bha

gann

aet

al.,

2010

;Cra

yet

al.,

2013

);an

dot

her

arom

atic

s,al

coho

ls,

amid

esan

dsp

ecifi

csa

ltsca

use

chao

trop

e-in

duce

dw

ater

stre

ss(H

alls

wor

thet

al.,

2003

a;C

ray

etal

.,20

13).

b.

Rel

ativ

eto

no-a

dded

stre

ssor

cont

rols

(see

Hal

lsw

orth

etal

.,20

03a)

.c.

Log

P>

1.95

(see

Bha

gann

aet

al.,

2010

;C

ray

etal

.,20

13).

d.

The

seda

taw

ere

take

nfr

omB

haga

nna

and

colle

ague

s(2

010)

;P.

putid

aK

T24

40(D

SM

Z61

25)

was

grow

nin

am

inim

alm

iner

al-s

alt

brot

h(w

ithgl

ucos

ean

dN

H4C

las

the

sole

carb

onan

dni

trog

ensu

bstr

ates

resp

ectiv

ely;

see

Har

tman

set

al.,

1989

;B

haga

nna

etal

.,20

10)

at30

°C.

The

med

iafo

rco

ntro

ltre

atm

ents

had

nost

ress

ors

adde

d.S

ome

P.pu

tida

stra

ins

can

tole

rate

benz

ene

atup

to20

mM

(Vol

kers

etal

.,20

10).

e.T

hepe

stic

ide

g-he

xach

loro

cycl

ohex

ane

(g-H

CH

)is

also

know

nas

linda

ne.

f.P

seud

omon

aspu

tida

KT

2440

was

grow

nin

mod

ified

Luria

–Ber

tani

brot

hat

30°C

;str

esso

rsw

ere

inco

rpor

ated

into

med

iapr

ior

toin

ocul

atio

n,an

dgr

owth

rate

sca

lcul

ated

,as

desc

ribed

byH

alls

wor

than

dco

lleag

ues

(200

3a).

The

med

iafo

rco

ntro

ltre

atm

ents

had

nost

ress

ors

adde

d.g

.Tw

een®

80w

asus

edas

am

odel

subs

titut

efo

rbi

osur

fact

ants

(Cra

yet

al.,

2013

).h

.T

hese

data

wer

eta

ken

from

Hal

lsw

orth

and

colle

ague

s(2

003a

);P.

putid

aK

T24

40w

asgr

own

inm

odifi

edLu

ria–B

erta

nibr

oth

at30

°Cas

desc

ribed

info

otno

te(f

).i.

Ext

rapo

late

dva

lues

.j.

Gly

cero

lis

ano

tabl

eex

cept

ion

(Will

iam

san

dH

alls

wor

th,

2009

).



Tab

le3.

Str

ess

tole

ranc

ean

den

ergy

gene

ratio

n:ce

llula

rch

arac

teris

tics

that

cont

ribut

eto

wee

d-lik

ebe

havi

our.a

Met

abol

ites,

prot

eins

,m

olec

ular

char

acte

ristic

s,an

dot

her

trai

tsF

unct

ion(

s)P

heno

typi

ctr

aits

Not

esan

dre

fere

nces

Tole

ran

ces

tom

ult

iple

envi

ron

men

tal

stre

sses

Abi

lity

tose

lect

from

anar

ray

offu

nctio

nally

dive

rse

com

patib

leso

lute

sin

resp

onse

tosp

ecifi

cst

ress

para

met

ers

Spe

cific

com

patib

leso

lute

sca

npr

otec

tag

ains

tos

mot

icst

ress

,te

mpe

ratu

reex

trem

es,

free

zing

,de

hydr

atio

nan

dre

hydr

atio

n,ch

aotr

opic

ity,

and/

orhy

drop

hobi

cst

ress

ors

(Cro

we

etal

.,19

84;

Bro

wn,

1990

;H

alls

wor

thet

al.,

2003

b;B

haga

nna

etal

.,20

10;

Chi

net

al.,

2010

;B

elle

tal,

2013

)

Abi

lity

tom

aint

ain

func

tiona

lity

ofm

acro

mol

ecul

arsy

stem

san

d/or

cell

turg

orun

der

dive

rse

stre

sses

Som

em

icro

bes

utili

zea

wid

ear

ray

ofco

mpa

tible

solu

tes

depe

ndin

gon

the

type

and

seve

rity

ofst

ress

;e.

g.P

seud

omon

aspu

tida

isex

cept

iona

lam

ong

bact

eria

inits

abili

tyto

synt

hesi

zean

dac

cum

ulat

epr

otec

tant

sas

dive

rse

asbe

tain

e,pr

olin

e,N

-ace

tylg

luta

min

ylgl

utam

ine

amid

e,gl

ycer

ol,

man

nito

land

treh

alos

e(D

’Sou

za-A

ult

etal

.,19

93;

Ket

set

al.,

1996

;B

haga

nna

etal

.,20

10);

Sac

char

omyc

esce

revi

siae

can

accu

mul

ate

prol

ine,

glyc

erol

and

treh

alos

e(s

eeTa

ble

6;K

aino

and

Taka

gi,

2008

).Li

keot

her

fung

i,A

sper

gillu

ssp

ecie

sut

ilize

ara

nge

ofpo

lyol

sas

wel

las

treh

alos

e(H

alls

wor

than

dM

agan

,19

94c;

Hal

lsw

orth

etal

.,20

03b)

but

thei

rex

cept

iona

labi

lity

toge

nera

teen

ergy

unde

rst

ress

(see

belo

w)

may

aid

glyc

erol

rete

ntio

nan

dth

ereb

yex

tend

ing

the

grow

thw

indo

wat

low

wat

erac

tivity

(Hoc

king

,19

93;

Will

iam

san

dH

alls

wor

th,

2009

)U

preg

ulat

ion

ofpr

otei

n-st

abili

zatio

npr

otei

nsin

com

bina

tions

tailo

red

tosp

ecifi

cst

ress

esb

Inad

ditio

nto

stre

ssor

s(in

clud

ing

thos

eof

biot

icor

igin

;Ta

ble

6),

prot

ein-

stab

iliza

tion

prot

eins

also

prot

ect

agai

nst

pert

urba

tions

indu

ced

byst

ress

essu

chas

tem

pera

ture

extr

emes

and

desi

ccat

ion

(Ars

ène

etal

.,20

00;

Fer

rer

etal

.,20

03)

Mai

nten

ance

ofpr

otei

nst

ruct

ure

and

func

tion

durin

gen

viro

nmen

tal

chal

leng

es

Sev

eral

stud

ies

show

high

lyef

ficie

ntre

spon

ses

ofP.

putid

ato

chao

trop

ican

dhy

drop

hobi

cst

ress

ors

via

upre

gula

tion

ofbe

twee

n10

and

20pr

otei

n-st

abili

zing

prot

eins

(Hal

lsw

orth

etal

.,20

03a;

San

tos

etal

.,20

04;

Seg

ura

etal

.,20

05;

Dom

íngu

ez-C

ueva

set

al.,

2006

;Ts

irogi

anni

etal

.,20

06;

Vol

kers

etal

.,20

06;

Bal

lers

tedt

etal

.,20

07).

The

Pal

Apr

otei

nin

Asp

ergi

llus

nidu

lans

indu

ces

ara

pid

upre

gula

tion

ofpr

otei

n-st

abili

zatio

npr

otei

nsin

resp

onse

toex

trem

epH

(Fre

itas

etal

.,20

11);

high

prod

uctio

nra

tes

ofpr

otei

n-st

abili

zatio

npr

otei

nsen

hanc

eto

lera

nce

toch

aotr

opic

salts

and

alco

hols

inS

.cer

evis

iae

and

Lact

obac

illus

plan

taru

m,

tohy

drop

hobi

cst

ress

ors

inS

.cer

evis

iae

and

Esc

heric

hia

coli

(for

refe

renc

es,

see

Bha

gann

aet

al.,

2010

),an

dlo

wte

mpe

ratu

re,

salt

and

othe

rst

ress

esin

Rho

doto

rula

muc

ilagi

nosa

(Lah

avet

al.,

2004

)In

trac

ellu

lar

accu

mul

atio

nof

ions

for

osm

otic

adju

stm

ent;

intr

acel

lula

rpr

otei

nsst

ruct

ural

lyad

apte

dto

high

ioni

cst

reng

th

The

utili

zatio

nof

ions

for

osm

otic

adju

stm

ent

avoi

dsth

een

ergy

-exp

ensi

vesy

nthe

sis

ofor

gani

cco

mpa

tible

solu

tes

(Kus

hner

,19

78;

Ore

n,19

99)

Abi

lity

tom

aint

ain

met

abol

icac

tivity

athi

ghex

tra-

and

intr

acel

lula

rio

nic

stre

ngth

Hal

oqua

drat

umw

alsb

yi,

and

Sal

inib

acte

rru

ber

(unu

sual

lyfo

ra

bact

eriu

m),

utili

zeth

eso

-cal

led

‘sal

t-in

’str

ateg

y(O

ren

etal

.,20

02;

Bar

davi

dan

dO

ren,

2012

;S

aum

etal

.,20

12)

Div

erse

prot

eins

and

path

way

sco

nfer

ring

tole

ranc

eto

solv

ents

,ch

aotr

opic

solu

tes

and

hydr

opho

bic

stre

ssor

s

Sol

vent

-tol

eran

tsp

ecie

ssu

chas

P.pu

tida

can

func

tion

athi

ghco

ncen

trat

ions

ofch

aotr

opic

and

hydr

opho

bic

stre

ssor

sdu

eto

the

colle

ctiv

eac

tiviti

esof

solv

ent

pum

psth

atex

pels

olve

ntm

olec

ules

,pa

thw

ays

that

cata

boliz

eth

eso

lven

t,m

embr

ane-

stab

iliza

tion

prot

eins

(see

belo

w),

com

patib

leso

lute

s(s

eeab

ove)

,an

dad

ditio

nalc

haot

rope

-an

dso

lven

t-st

ress

resp

onse

s(R

amos

etal

.,20

02;

Tim

mis

,20

02;

Hal

lsw

orth

etal

.,20

03a;

Vol

kers

etal

.,20

06;

Bha

gann

aet

al.,

2010

;F

illet

etal

.,20

12)

Hig

hto

lera

nce

toch

aotr

opic

and

hydr

opho

bic

solv

ent

stre

ssor

s

Due

toits

exce

ptio

nals

olve

ntto

lera

nce

P.pu

tida

isth

eor

gani

smof

choi

cefo

rm

any

indu

stria

lapp

licat

ions

incl

udin

gbi

otra

nsfo

rmat

ion

intw

o-ph

ase

syst

ems

and

bior

emed

iatio

n(T

imm

is,

2002

).

Mem

bran

e-st

abili

zatio

npr

otei

ns;

e.g.

cis/

tran

s-is

omer

ase

(CT

I)M

embr

ane

stab

iliza

tion

unde

rst

ress

Enh

ance

dto

lera

nce

tost

ress

esth

atim

pact

mem

bran

est

ruct

ure

Sev

eral

prot

eins

are

invo

lved

inm

aint

aini

ngbi

laye

rrig

idity

inP.

putid

adu

ring

expo

sure

toto

luen

ean

dot

her

solv

ents

orhy

drop

hobi

cst

ress

ors

(Ber

nale

tal.,

2007

)P

rote

ins

invo

lved

inth

em

oder

atio

nof

mem

bran

eflu

idity

Mai

nten

ance

ofm

embr

ane

fluid

ityan

dm

embr

ane-

asso

ciat

edpr

oces

ses

unde

rco

nditi

ons

such

aslo

wte

mpe

ratu

re(T

urk

etal

.,20

11)

Enh

ance

dto

lera

nce

todi

vers

e,ph

ysic

oche

mic

alst

ress

para

met

ers

For

exam

ple

Aur

eoba

sidi

umpu

llula

ns,

Cry

ptoc

occu

sliq

uefa

cien

san

dR

.muc

ilagi

nosa

(Tur

ket

al.,

2011

)



Pro

mot

er(s

)th

atsi

mul

tane

ousl

yco

ntro

lmul

tiple

stre

ss-r

espo

nse

gene

s,e.

g.st

ress

-res

pons

eel

emen

ts(S

TR

Es)

Act

ivat

ion

ofm

ultip

lece

llula

rst

ress

-res

pons

esE

nhan

ced

tole

ranc

eto

mul

tiple

stre

ss-p

aram

eter

sT

hetr

ansc

riptio

nfa

ctor

s(M

sn2p

and

Msn

4p)

invo

lved

inS

TR

E-m

edia

ted

stre

ssre

spon

ses

inS

.cer

evis

iae

accu

mul

ate

inth

enu

cleu

sup

onhe

at-,

etha

nol-

(cha

otro

pe-)

,an

dos

mot

ical

lyin

duce

dst

ress

es,

and

durin

gnu

trie

ntlim

itatio

n.T

heS

TR

Eis

upst

ream

ofge

nes

for

prot

ein-

stab

iliza

tion

prot

eins

(see

abov

e)m

etab

olic

enzy

mes

,an

dce

llula

ror

gani

zatio

npr

otei

ns(G

örne

ret

al.,

1998

;M

oskv

ina

etal

.,19

98)

Pro

tein

sin

volv

edin

DN

Apr

otec

tion

unde

rst

ress

;e.

g.D

NA

-bin

ding

prot

ein

(Dps

)F

orm

atio

nof

apr

otei

n:ch

rom

osom

eco

mpl

exth

atpr

otec

tsD

NA

Enh

ance

dD

NA

stab

ility

and

redu

ced

risk

ofm

utat

ion

inre

latio

nto

mul

ti-fa

rious

stre

sses

The

role

ofD

psha

sbe

enw

ell-c

hara

cter

ized

inE

.col

iin

rela

tion

todi

vers

een

viro

nmen

talc

halle

nges

incl

udin

gre

activ

eox

ygen

spec

ies,

iron

and

copp

erto

xici

ty,

ther

mal

stre

ssan

dex

trem

esof

pH(N

air

and

Fin

kel,

2004

)P

athw

ays

for

synt

hesi

sof

caro

teno

ids

(e.g

.b-

caro

tene

inD

unal

iella

salin

a;to

rula

rhod

inin

Rho

doto

rula

spp.

)

Car

oten

oids

abso

rblig

htan

dth

ereb

ypr

otec

tce

llula

rm

acro

mol

ecul

esan

dor

gane

lles

from

expo

sure

toul

trav

iole

t

Tole

ranc

eof

expo

sure

toul

trav

iole

tirr

adia

tion

Syn

thes

isof

b-ca

rote

neis

upre

gula

ted

inre

spon

seto

light

inD

.sal

ina

(Che

nan

dJi

ang,

2009

);ca

rote

noid

sar

eco

ncen

trat

edin

the

plas

ma

mem

bran

eof

S.r

uber

(Ant

ónet

al.,

2002

);st

udie

sof

R.m

ucila

gino

sash

owth

atto

rula

rhod

inen

hanc

esto

lera

nce

toul

trav

iole

tB

expo

sure

(Mol

iné

etal

.,20

10)

Pre

fere

ntia

lutil

izat

ion

ofa

chao

trop

icco

mpa

tible

solu

teat

high

NaC

lcon

cent

ratio

nan

d/or

low

tem

pera

ture

Rig

idifi

catio

nof

mac

rom

olec

ular

stru

ctur

esat

high

NaC

lan

dlo

wte

mpe

ratu

reca

nin

duce

met

abol

icin

hibi

tion

(Bro

wn,

1990

;F

erre

ret

al.,

2003

;C

hin

etal

.,20

10)

that

can

beco

mpe

nsat

edfo

rby

glyc

erol

and/

orfr

ucto

se(B

row

n,19

90;

Chi

net

al.,

2010

)

Enh

ance

dto

lera

nce

toex

trem

eco

nditi

ons

that

rigid

ifym

acro

mol

ecul

arsy

stem

s

The

high

intr

acel

lula

rco

ncen

trat

ions

ofgl

ycer

olin

D.s

alin

aun

der

salt

stre

ssan

dgl

ycer

olan

d/or

fruc

tose

inan

dA

sper

gillu

san

dE

urot

ium

spp.

and

R.m

ucila

gino

saat

low

tem

pera

ture

are

able

toex

tend

grow

thw

indo

ws

unde

rth

ese

extr

eme

cond

ition

s(B

row

n,19

90;

Laha

vet

al.,

2002

;C

hin

etal

.,20

10).

Dun

alie

llasa

lina

has

mem

bran

esw

ithre

duce

dgl

ycer

olpe

rmea

bilit

yth

ereb

yai

ding

rete

ntio

nof

this

com

patib

leso

lute

(Bar

davi

det

al.,

2008

)E

ffici

ent

syst

emto

elim

inat

efr

eera

dica

ls(s

eeab

ove)

Elim

inat

ion

ofre

activ

eox

ygen

spec

ies

(see

also

Tabl

e5)

Var

ious

subs

tanc

esan

dst

ress

para

met

ers

can

indu

ceox

idat

ive

stre

ss

Div

erse

envi

ronm

enta

lsub

stan

ces

and

para

met

ers

indu

ceox

idat

ive

stre

ss,

eith

erdi

rect

lyor

indi

rect

ly(e

.g.

via

lipid

pero

xida

tion)

.F

orex

ampl

e,ch

aotr

opic

stre

ssor

san

dhe

atsh

ock

have

been

asso

ciat

edw

ithth

ein

duct

ion

ofox

idat

ive

stre

ssre

spon

ses

inS

.cer

evis

iae

and

P.pu

tida

(Cos

taet

al.,

1997

;H

alls

wor

thet

al.,

2003

a)P

rote

ins

asso

ciat

edw

ithre

gula

tion

ofcy

toso

licpH

;e.

g.th

ely

sine

deca

rbox

ylas

esy

stem

(cod

edfo

rby

the

cadB

Aop

eron

);th

eN

a+ /H

+

antip

orte

r

Con

vers

ion

and

expo

rtof

lysi

ne/c

adav

erin

eth

atre

sults

inin

crea

sed

pHof

the

cyto

soli

nba

cter

ia(Á

lvar

ez-O

rdóñ

ezet

al.,

2011

);th

eN

a+ /H

+an

tipor

ter

Nha

1de

crea

ses

intr

acel

lula

rhy

drog

enio

nco

ncen

trat

ion

Tole

ranc

eof

low

-pH

envi

ronm

ents

Dec

arbo

xyla

sesy

stem

sth

atin

crea

sein

trac

ellu

lar

pHal

soex

ist

for

othe

ram

ino

acid

s(Á

lvar

ez-O

rdóñ

ezet

al.,

2011

);N

ha1

grea

tlyen

hanc

esvi

abili

tyof

Sac

char

omyc

esbo

ular

diia

tpH

2(d

osS

anto

sS

ant’A

naet

al.,

2009

)

Mul

tidru

gef

flux

pum

ps(f

orde

tails

see

Tabl

e6)

Enz

ymes

for

synt

hesi

sof

extr

acel

lula

rpo

lym

eric

subs

tanc

esP

rodu

ctio

nan

dse

cret

ion

ofpo

lym

eric

subs

tanc

esE

nhan

ced

tole

ranc

eto

mul

tiple

stre

ssor

san

dst

ress

para

met

ers

Ext

race

llula

rpo

lym

eric

subs

tanc

esha

vebe

ensh

own

toco

nfer

prot

ectio

nto

E.c

olic

ells

expo

sed

tohi

ghte

mpe

ratu

re,

low

pH,

salt

and

oxid

ativ

est

ress

(Che

net

al.,

2004

),an

dar

eas

soci

ated

with

stre

sspr

otec

tion

inC

lost

ridiu

msp

p.,

Pan

toea

anan

atis

,P.

putid

aan

dot

her

Pse

udom

onas

spp.

(Cha

nget

al.,

2007

;M

oroh

oshi

etal

.,20

11;

see

also

Tabl

e6)

Upr

egul

atio

nof

prot

eins

invo

lved

inpr

otei

nsy

nthe

sis

unde

rst

ress

Toen

hanc

eor

mai

ntai

nth

equ

antit

y,ty

pe,

and

func

tiona

lity

ofce

llula

rpr

otei

nsun

der

stre

ssM

aint

enan

ceof

the

cellu

lar

syst

eman

dits

met

abol

icac

tivity

unde

rst

ress

Can

beup

regu

late

din

resp

onse

tost

ress

indu

ced

byhi

ghte

mpe

ratu

re,

chao

trop

icso

lute

s,hy

drop

hobi

cst

ress

ors

and

othe

rst

ress

para

met

ers

(e.g

.P.

putid

a;H

alls

wor

thet

al.,

2003

a;V

olke

rset

al.,

2009

)P

olyp

loid

y,an

eupl

oidy

,as

soci

atio

nw

ithpl

asm

ids,

and/

orhy

brid

izat

ion

that

enha

nce(

s)st

ress

tole

ranc

e

Whe

reas

hybr

idiz

atio

n,po

lypl

oidy

,an

eupl

oidy

and

asso

ciat

ion

with

plas

mid

sca

nbe

ecol

ogic

ally

disa

dvan

tage

ous,

such

trai

tsca

nen

hanc

eth

evi

gour

,st

ress

tole

ranc

ean

dco

mpe

titiv

eab

ility

ofso

me

mic

robe

ssu

chas

Pic

hia

spp.

,S

.cer

evis

iae,

P.pu

tida

and

S.r

uber

(Tab

le1;

Rai

nier

ieta

l.,19

99;

Nau

mov

etal

.,20

01;

Mon

godi

net

al.,

2005

;Ta

rket

al.,

2005

;D

har

etal

.,20

11;

Che

net

al.,

2012

)

Enh

ance

dst

ress

tole

ranc

eA

neup

loid

cells

ofS

.cer

evis

iae

have

enha

nced

tole

ranc

eto

oxid

ativ

est

ress

and

dive

rse

inhi

bito

rsof

bioc

hem

ical

proc

esse

s(C

hen

etal

.,20

12);

poly

ploi

dyca

nen

hanc

evi

gour

and

stre

ssto

lera

nce

inso

me

spec

ies

(see

also

Tabl

es1

and

5);

the

stre

ssto

lera

nce

ofso

me

mic

robi

alw

eeds

isen

hanc

edby

thei

ras

soci

atio

nw

ithpl

asm

ids

(e.g

.th

eP.

putid

ato

l-pla

smid

that

enha

nces

solv

ent

tole

ranc

e;Ta

rket

al.,

2005

;D

omín

guez

-Cue

vas

etal

.,20

06;

the

S.r

uber

plas

mid

cont

ains

age

nein

volv

edin

ultr

avio

let

prot

ectio

n;M

ongo

din

etal

.,20

05)



Tab

le3.

cont

.

Met

abol

ites,

prot

eins

,m

olec

ular

char

acte

ristic

s,an

dot

her

trai

tsF

unct

ion(

s)P

heno

typi

ctr

aits

Not

esan

dre

fere

nces

Pol

yext

rem

ophi

licgr

owth

-phe

noty

peA

bilit

yto

grow

optim

ally

unde

rm

ultip

le,

extr

eme

cond

ition

s;e.

g.ex

trem

ely

acid

and

alka

li(p

H2–

10),

high

-sal

t(2

.5M

NaC

l),an

dlo

w-t

empe

ratu

reco

nditi

ons

(Lah

avet

al.,

2002

;Li

bkin

dan

dS

ampa

io,

2010

)

Pol

yext

rem

ophi

leR

hodo

toru

lam

ucila

gino

sais

capa

ble

ofgr

owth

over

anin

cred

ible

rang

eof

phys

icoc

hem

ical

cond

ition

s(in

clud

ing

alm

ost

the

entir

epH

rang

efo

rm

icro

bial

life)

and

isab

leto

colo

nize

aco

rres

pond

ingl

yw

ide

dive

rsity

ofen

viro

nmen

ts(f

orex

ampl

esse

em

ain

text

)G

enes

asso

ciat

edw

ithsa

ltst

ress

Sug

arca

tabo

lism

(e.g

.R

mP

GM

2,R

mG

PA

2,R

mA

CK

1,R

mM

CP

1an

dR

mP

ET

9),

prot

ein

glyc

osyl

atio

n(e

.g.

Rm

SE

C53

),ar

omat

icam

ino

acid

synt

hesi

s(e

.g.

Rm

AR

O4)

,re

gula

tion

ofpr

otei

nsy

nthe

sis

(e.g

.R

mA

NB

1)

Mai

nten

ance

ofpr

otei

nsy

nthe

sis

and

ener

gyge

nera

tion

unde

rsa

ltst

ress

Bet

wee

n10

and

20ge

nes

are

invo

lved

inin

crea

sed

tole

ranc

eto

NaC

lan

d/or

LiC

lin

R.m

ucila

gino

sa(L

ahav

etal

.,20

04;

Gos

tinca

ret

al.,

2012

)

Met

abol

ites

asso

ciat

edw

ithre

sist

ance

toan

timic

robi

alpl

ant

met

abol

ites

and

surv

ival

inph

yllo

sphe

reha

bita

ts

Met

abol

ites

invo

lved

inqu

orum

sens

ing

may

enha

nce

com

petit

ive

abili

tyon

the

leaf

surf

ace

Enh

ance

dsu

rviv

alan

dco

mpe

titiv

eab

ility

By

cont

rast

toot

her

phyl

losp

here

mic

robe

s,P.

anan

atis

isre

sist

ant

toth

ein

hibi

tory

effe

cts

ofpl

ant

alka

loid

san

dth

isco

rrel

ates

with

the

prod

uctio

nof

met

abol

ites

invo

lved

inqu

orum

sens

ing

such

asN

-acy

l-hom

oser

ine

lact

one

(Eny

aet

al.,

2007

)H

igh

-eff

icie

ncy

ener

gy-

gen

erat

ion

syst

ems

Ligh

t-ac

tivat

edpr

oton

pum

ps(e

.g.

xant

horh

odop

sin)

Toge

nera

tea

prot

on-m

otiv

efo

rce,

utili

zing

light

asan

ener

gyso

urce

Util

izat

ion

oflig

htfo

rtr

ansm

embr

ane

prot

ontr

ansp

ort

Xan

thor

hodo

psin

,fo

und

inS

.rub

er,

isa

prot

onpu

mp

mad

eup

oftw

och

rom

opho

res;

alig

ht-a

bsor

bing

caro

teno

idan

da

prot

ein

(Bal

asho

vet

al.,

2005

);a

light

-act

ivat

edpr

oton

pum

pw

asal

sore

cent

lyde

scrib

edin

H.w

alsb

yi(L

obas

soet

al.,

2012

)H

igh

expr

essi

onof

gene

sin

volv

edin

ener

gyge

nera

tion

(e.g

.fb

a,py

kF,

atpA

and

atpD

c )R

apid

cata

bolis

mof

carb

onsu

bstr

ates

lead

ing

toen

hanc

edsy

nthe

sis

ofA

TP

Effi

cien

ten

ergy

-gen

erat

ion

Hig

hex

pres

sion

ofE

.col

igen

esfb

a,py

kF,

atpA

and

atpD

can

beas

soci

ated

with

abili

tyto

grow

rapi

dly,

enha

nced

stre

ssto

lera

nce

and

–by

impl

icat

ion

–gr

eate

rco

mpe

titiv

eab

ility

(Kar

linet

al.,

2001

)E

nhan

ced

ener

gy-e

ffici

ency

atlo

wnu

trie

ntco

ncen

trat

ions

(e.g

.se

egl

utam

ate

dehy

drog

enas

een

try

inTa

ble

5)U

preg

ulat

ion

ofpr

otei

nsin

volv

edin

ener

gyge

nera

tion

unde

rch

aotr

opic

and

solv

ent-

indu

ced

(hyd

roca

rbon

)st

ress

es(H

alls

wor

thet

al.,

2003

a;V

olke

rset

al.,

2006

).

Mai

nten

ance

ofen

ergy

gene

ratio

ncl

ose

toth

epo

int

ofsy

stem

failu

reun

der

host

ileco

nditi

ons

Effi

cien

ten

ergy

gene

ratio

ndu

ring

pote

ntia

llyle

thal

chal

leng

es

The

exce

ptio

nala

bilit

yof

P.pu

tida

tore

spon

dan

dad

apt

toch

aotr

opic

,so

lven

tan

dhy

droc

arbo

nst

ress

ors

has,

inpa

rt,

been

attr

ibut

edto

cons

ider

able

incr

ease

sin

ener

gy-

and

NA

D(P

)H-g

ener

atin

gsy

stem

s

Idio

sync

ratic

geno

me

mod

ifica

tions

asso

ciat

edw

ithre

info

rced

ener

gym

etab

olis

mE

nhan

ced

prim

ary

met

abol

ism

and

ener

gy-g

ener

atio

nsy

stem

sE

nhan

ced

vigo

uran

den

ergy

prod

uctio

nA

sper

gillu

ssp

ecie

sha

venu

mer

ous

geno

me

mod

ifica

tions

,su

chas

gene

dupl

icat

ions

for

pyru

vate

dehy

drog

enas

e,ci

trat

esy

ntha

se,

acon

itase

and

mal

ate

dehy

drog

enas

eth

aten

hanc

epr

imar

ym

etab

olis

min

clud

ing

glyc

olys

isan

dth

eT

CA

cycl

e(F

lipph

ieta

l.,20

09)

Effi

cien

tut

iliza

tion

ofin

trac

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lar

rese

rves

for

ener

gyge

nera

tion

Cat

abol

ism

ofst

ored

subs

tanc

esto

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tion

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cond

ary

met

abol

ites,

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ility

and/

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her

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tions

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lity

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ain

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nditi

ons

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cien

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5)an

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tion

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erat

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ers

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titiv

ead

vant

age

inS

.cer

evis

iae

and

othe

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ecie

s(C

astr

olet

al.,

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;K

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riet

al.,

2005

)C

onco

mita

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ergy

gene

ratio

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dsy

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ofan

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with

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lesy

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ngth

ech

aotr

opic

stre

ssor

etha

nol(

see

Tabl

e6)

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rgy

gene

ratio

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ked

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nthe

sis

ofan

antim

icro

bial

Eac

hgl

ucos

em

olec

ule

ferm

ente

dby

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isia

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estw

oet

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lm

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ules

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mol

ecul

esof

AT

P(P

išku

ret

al.,

2006

)

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that

can

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soci

ated

with

and

give

rise

tow

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ness

;the

cate

gorie

sof

trai

tsar

eno

tmut

ually

excl

usiv

e.In

divi

dual

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tsm

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tbe

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wev

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oryzae, up to ~ 4 M NaCl or KCl (Hallsworth et al., 1998).Aspergillus (and Eurotium) strains are capable of reason-able growth rates close to 0°C (Chin et al., 2010), andsome reports suggests that the biotic windows for someAspergillus species ultimately fail at � -18°C (Vallentyne,1963; Siegel and Speitel, 1976). Whereas a number ofcomparable fungal genera show moderate levels of stresstolerance, Aspergillus species generally out-perform theircompetitors and top numerous league tables for asco-mycete stress tolerance (see Pitt, 1975; Wheeler andHocking, 1993; Williams and Hallsworth, 2009).

Studies of seven Aspergillus species have revealed anumber of genome modifications within this genus thatreinforce both primary metabolism and energy generation(Table 3; Flipphi et al., 2009). These include gene dupli-cations for key enzymes that control metabolic flux, suchas pyruvate dehydrogenase, citrate synthase, aconitase,and malate dehydrogenase that enhance glycolysis andthe TCA cycle (Flipphi et al., 2009). There is evidencethat, at the low water activities (high osmotic pressures)associated with very high-salt and high-sugar habitats,the biotic window of xerophilic fungi fail due to the pro-hibitive energy expenditure required to prevent the highlevels of intracellular glycerol from leaking out of the mem-brane (Hocking, 1993). The adaptability and competitiveability of Aspergillus species (most of which can alsoproliferate under non-extreme conditions) may be attrib-uted, in part, from enhanced energy-generating capability.Aspergillus species (like many fungi) can utilize a range ofpolyols – as well as trehalose – as compatible solutesbased on their individual strengths as protectants againstosmotic stress, desiccation rehydration, chaotropes etc.(Crowe et al., 1984; Brown, 1990; Hallsworth et al.,2003b). Aspergillus and Eurotium strains can also accu-mulate chaotropic sugars from the medium, or preferen-tially synthesize and accumulate chaotropic glycerol, inorder to enhance growth at temperatures below ~ 10°C(Chin et al., 2010; see also below).

Salinibacter ruber is a halophilic bacterium found inhigh numbers at molar salt concentrations in aerobicaquatic habitats that are otherwise more densely popu-lated by archaeal than bacterial species. Unusually for abacterium, S. ruber takes in ions to use as compatiblesolutes and thereby avoids synthesis of organic compat-ible solutes that would be energetically unfavourable inenvironments of > 1 M NaCl (Oren, 1999) and hasevolved intracellular proteins that are both structurallystable and catalytically functional in the cytosol at highionic strength (Table 3). Salinibacter ruber (as well as thealga Dunaliella salina and yeast R. mucilaginosa) accu-mulates carotenoids in response to light which can protectagainst oxidative stress that is a potential hazard in salt-erns exposed to high levels of ultraviolet (Table 3). Halo-quadratum walsbyi, an Archaeon that is also a dominant

player in saltern communities (Table S1), also uses the‘salt-in’ compatible-solute strategy, and – along withS. ruber – has light-activated protein pumps that generateproton-motive force and thereby boost energy generation(Table 3). In addition, H. walsbyi is unusually tolerant tothe chaotropic salt MgCl2 that can reach high concentra-tions in evaporate ponds (Hallsworth et al., 2007; Bar-david et al., 2008). Dunaliella salina is also highlyprevalent in saline habitats that (unusually for an alga)can successfully compete with the multitude of halophilicArchaea found in 5 M NaCl environments (see later;Table S1). This alga preferentially utilizes glycerol as acompatible solute, is able to accumulate glycerol to molarconcentrations (6–7 M; see Bardavid et al., 2008), andhas low membrane permeability to this compatible-solutethus aiding retention (Bardavid et al., 2008).

Glycerol is unique in its ability to maintain the flexibilityof macromolecular structures under conditions that wouldotherwise cause excessive rigidification, e.g. molar con-centrations of NaCl, or low temperature (Back et al.,1979; Hallsworth et al., 2007; Williams and Hallsworth,2009; Chin et al., 2010). Species able to grow at low orsubzero temperatures (e.g. Aspergillus, Cryptococcus,Rhodotorula species, including R. mucilaginosa) eitherprimarily use glycerol as a compatible solute or preferen-tially accumulate this chaotrope at low temperature(Table 3; Lahav et al., 2004; Chin et al., 2010). Rhodo-torula mucilaginosa is able to colonize – and frequentlydominates – diverse substrates/environments includingsaline and non-saline soils, aquatic habitats (both liquid-and ice-associated), the acidic surface-film of sphagnummoss (as well as other plant tissues) and various sur-faces within the human body and other animals(Table S1; Egan et al., 2002; Trindade et al., 2002; Vitalet al., 2002; Lahav et al., 2002; 2004; Lisichkina et al.,2003; Buzzini et al., 2005; Perniola et al., 2006; Goyalet al., 2008; Turk et al., 2011; Kachalkin and Yurkov,2012). This ability is coupled with an exceptional level oftolerance to multiple stresses: R. mucilaginosa is (highlyunusual for a yeast) a polyextremophile that is psy-chrophilic, highly salt-tolerant, and can growth over themajority of the pH range known to support microbial life(i.e. < 2 and > 10, see Table 3; Lahav et al., 2002).

Some microbial habitats such as fruits that have beendisconnected from the vascular system (and immuneresponses) of the parent plant have a favourable wateractivity and high nutrient availability and are thereforepotentially habitable by a wide range of microbes(Ragaert et al., 2006). As the microbial community devel-ops on a detached fruit (or in apple or grape musts; seeTable S1) there can be changes in the composition andconcentration of sugars, osmolarity, water activity, ethanolconcentration (and that of other antimicrobials), pH andother environmental factors that are severe enough to



inhibit or eliminate most members of the original micro-flora (see Brown, 1990; Hallsworth, 1998; de Pina andHogg, 1999; Pretorius, 2000; Bhaganna et al., 2010). Theyeast S. cerevisiae that is relatively scarce in natural habi-tats (and even when present forms a quantitatively insig-nificant component of the natural community; Renoufet al., 2005; Raspor et al., 2006) is unsurpassed in itsability to emerge to dominate high-sugar habitats at wateractivities above 0.9 (Table S1; Hallsworth, 1998; Preto-rius, 2000). We therefore compared its tolerance towardsa range of habitat-relevant stressors with those of 12other yeasts that occur at the insect–flower interface, onplant tissues, and/or are environmentally widespread(Fig. 2; Table 4). This experiment revealed that S. cerevi-siae has a more vigorous growth phenotype and morerobust stress tolerance than the other species tested withthe exception of two species of Pichia, another genuscharacterized by weed-like traits (see Fig. 2; Table 4).Stress phenotypes of the yeasts assayed were comparedon the basis of stressor type and mechanistically distinctstress-parameters in order to assess resilience to both thedegree and diversity of environmental challenges(Table 4). Under the assay conditions it was the threeS. cerevisiae strains, Pichia (Kodamaea) ohmeri andPichia sydowiorum that exhibited the greatest tolerance tothe widest range of solute-imposed stresses (Table 4).Other species studied were slow growers, have specificenvironmental requirements (e.g. the halotolerantD. hansenii and Hortaea werneckii), and/or otherwiselacked the capacity for vigorous growth on the high-sugarsubstrate at 30°C (see Fig. 2). Generally S. cerevisiaestrains were fast-growing, xerotolerant, and highlyresistant to chaotrope-induced, osmotic, matric andkosmotrope-induced stresses and are known to be acido-tolerant and capable of growth over a wide temperaturerange, from ~0°C to 45°C (Fig. 2A and B; Table 4).Although Pichia species can produce ethanol (P. anomalacan produce up to 0.36 M ethanol; Djelal et al., 2005)when growing side by side in high-sugar habitats withS. cerevisiae, Pichia species are unable to tolerate the

molar ethanol concentrations that S. cerevisiae canproduce (Lee et al., 2011).

Saccharomyces cerevisiae is metabolically wired toconcomitantly synthesize an antimicrobial chaotrope(ethanol), accumulate a compatible solute (glycerol) thataffords protection against this chaotrope (see below), andat the same time generate energy without any loss ofATP-generation efficiency (Table 3): a remarkable pheno-type that is coupled with the deployment of other compat-ible solutes under specific conditions (trehalose andproline). Trehalose, which can reach concentrations of upto 13% dry weight in S. cerevisiae (Aranda et al., 2004), ishighly effective at stabilizing macromolecular structuresthat are exposed to chaotropic substances (e.g. ethanol,2-phenylethanol) and enabling cells to survivedesiccation–rehydration cycles (Crowe et al., 1984;Mansure et al., 1994). The highest reported tolerance toethanol stress was in S. cerevisiae cells capable ofgrowth and metabolism up to 28% v/v (≡ 20% w/v or4.3 M; chaotropic activity = 25.3 kJ g-1; Hallsworth, 1998;Hallsworth et al., 2007) when the medium contained highconcentrations of a compatible solute, proline (Thomaset al., 1993); furthermore of the seven microbes reportedto have the highest resistance to other chaotropic sub-stances (including urea, phenol) the majority are weedspecies including A. wentii, S. cerevisiae, Escherichia coliand P. putida (Hallsworth et al., 2007).

The stress mechanisms for numerous types of cellularstress operate at the level of water:macromolecule inter-actions (Crowe, et al., 1984; Brown, 1990; Sikkema et al.,1995; Casadei et al., 2002; Ferrer et al., 2003; Hallsworthet al., 2003a; 2007; McCammick et al., 2009; Bhagannaet al., 2010; Chin et al., 2010). As front-line stress protect-ants, compatible solutes (within limits) can thereforemollify stress the inhibitory effects of an indefinite numberof stress parameters (see Crowe, et al., 1984; Brown,1990; Hallsworth et al., 2003b; Bhaganna et al., 2010;Chin et al., 2010; Bell et al., 2013) but cells also upregu-late other protection systems (see also above; Table 3). InS. cerevisiae, an extensive number of genes that code for

Fig. 2. Growth of Saccharomyces cerevisiae strains: (A) CCY-21-4-13, (B) Alcotec 8 and (C) CBS 6412 and other yeast species: (D) Candidaetchellsii (UWOPS 01–168.3), (E) Cryptococcus terreus (PB4), (F) Debaryomyces hansenii (UWOPS 05-230.3), (G) Hansenula (Ogataea)polymorpha (CBS 4732), (H) Hortaea werneckii (MZKI B736), (I) Kluyveromyces marxianus (CBS 712), (J) Pichia (Kodamaea) ohmeri(UWOPS 05-228.2), (K) Pichia (Komagataella) pastoris (CBS 704), (L) Pichia sydowiorum (UWOPS 03-414.2), (M) Rhodotorula creatinivora(PB7), (N) Saccharomycodes ludwigii (UWOPS 92–218.4) and (O) Zygosaccharomyces rouxii (CBS 732) on a range of media at 30°C. Thesewere: malt-extract, yeast-extract phosphate agar (MYPiA) without added solutes (control), and MYPiA supplemented with diverse stressors –ethanol, methanol, glycerol, fructose, sucrose, NaCl, MgCl2, ammonium sulfate, proline, xantham gum and polyethylene glycol (PEG) 8000 –over a range of concentrations as shown in key (values indicate %, w/v). A standard Spot Test was carried out (see Chin et al., 2010; Tohet al., 2001) that was modified from Albertyn and colleagues (1994) for stress phenotype characterization (see Table 5). Colony density wasassessed after an incubation time of 24 h on a scale of 0–5 arbitrary units (Chin et al., 2010). Cultures were obtained from (for strain A) theCulture Collection of Yeasts (CCY, Slovakia); (strain B) Hambleton Bard Ltd, Chesterfield, UK; (strains C, G, I, K, O) the Centraalbureau voorSchimmelcultures (CBS, the Netherlands); (strains D, F, J, L, N) the University of Western Ontario Plant Sciences Culture Collection (UWOPS,Canada); (strains E, M) were obtained from Dr Rosa Margesin, Institute of Microbiology, Leopold Franzens University, Austria; and (strain H)the Microbial Culture Collection of National Institute of Chemistry (MZKI, Slovenia). All Petri plates containing the same medium were sealedin a polythene bag to maintain water; all experiments were carried out in duplicate, and plotted values are the means of independenttreatments.



0 1 2 3 4 5 0 1 2 3 4 5 0 1 2 3 4 5

Spot density (arbitrary units)

A B C

D E F

G H I

J K L

M N O

none [control]ethanol (1)ethanol (5)ethanol (15)methanol (2)methanol (10)methanol (20)glycerol (10)glycerol (30)glycerol (50)fructose (10)fructose (30)fructose (55)sucrose (1)sucrose (1.7)sucrose (2.4)NaCl (1.5)NaCl (6)NaCl (8)MgCl2 (1)MgCl2 (6)MgCl2 (12)(NH4)2SO4 (3.3)(NH4)2SO4 (10)proline (0.01)proline (0.17)proline (0.29)xantham gum (0.1)xantham gum (0.3)xanthan gum (0.5)PEG (5)

Add

ed s

olut

e (c

once

ntra

tion,

% w

/v)



Tab

le4.

Str

ess

phen

otyp

esan

dec

ophy

siol

ogic

alpr

ofile

sof

Sac

char

omyc

esce

revi

siae

rela

tive

toth

ose

ofot

her

yeas

tsp

ecie

s.

Yeas

tsp

ecie

sa

Tole

ranc

eto

dive

rse

stre

ssor

sbTo

lera

nce

todi

stin

ctst

ress

mec

hani

smsb

Add

ition

alno

tes

onst

ress

and

grow

thph

enot

ypes

cTy

pica

lhab

itat

Eco

phys

iolo

gica

ldes

crip

tiond

Alc

ohol

sG

lyce

rol

Sug

ars

Sal

tsO

ther

sC

haot

ropi

cO

smot

icM

atric

Kos

mot

ropi

c

Sac

char

om

yces

cere

visi

aest

rain

CC

Y-21

-4-1

3H

ighe

rM

idH

ighe

rH

ighe

rH

ighe

rH

ighe

rH

ighe

rH

ighe

rH

ighe

rT

opt30

–35°

C;

Tm

in~0

.5°C

;T

max

45°C

pHop

t3–

7;pH

min

~2.5

e ;fa

stgr

ower

Fru

its;

othe

rfle

shy

plan

ttis

sues

;ne

ctar

Mul

tiple

stre

ssto

lera

nces

incl

udin

gsu

gar

and

etha

nolf ;

stre

ssp

hen

oty

pe

of

axe

roto

lera

nt,

acid

oto

lera

nt,

vig

oro

us

wee

dA

lcot

ec8

Hig

her

Mid

Mid

Mid

Hig

her

Hig

her

Mid

Hig

her

Mid

As

abov

eA

sab

ove

As

abov

eC

BS

6412

Hig

her

Mid

Hig

her

Mid

Hig

her

Hig

her

Mid

Hig

her

Mid

As

abov

eA

sab

ove

As

abov

eO

ther

spec

ies

(str

ain

)C

andi

daet

chel

lsii

(UW

OP

S01

–168

.3)

Low

erH

ighe

rM

idH

ighe

rM

ixed

Hig

her

Hig

her

Mid

Mid

Slo

wgr

ower

eP

ollin

atin

gin

sect

s;flo

wer

s;fe

rmen

ted

food

s

Into

lera

ntto

spec

ific

stre

ssor

s;sl

ow-g

row

ing

Cry

ptoc

occu

ste

rreu

s(P

B4)

Mid

Mid

Hig

her

Mid

Hig

her

Mid

Mid

Hig

her

Mid

Top

t10

°C;

Tm

in1°

Ce ;

slow

grow

erS

oils

and

sedi

men

ts;

subs

urfa

ceen

viro

nmen

ts

Asl

ow-g

row

ing

psyc

hrop

hile

g

Deb

aryo

myc

esha

nsen

ii(U

WO

PS

05–2

30.3

)M

idM

idH

ighe

rH

ighe

rH

ighe

rM

idM

idH

ighe

rLo

wer

Top

t30

–32°

C;

pHop

t5.

5e ;fa

stgr

ower

Hig

h-sa

lten

viro

nmen

tsan

dfo

ods

Hal

otol

eran

t;a

fast

-gro

win

ghi

gh-s

alt

spec

ialis

tH

anse

nula

(Oga

taea

)po

lym

orph

a(C

BS

4732

)H

ighe

rM

idM

idM

idH

ighe

rH

ighe

rLo

wer

Hig

her

Hig

her

Top

t37

–43°

C;

pHop

t4.

5–5.

5eS

oil,

inse

ctgu

t,fr

uit

juic

eN

eith

erfa

st-g

row

ing

nor

high

lyst

ress

tole

rant

;a

high

-tem

pera

ture

spec

ialis

tH

orta

eaw

erne

ckii

(MZ

KI

B73

6)M

idM

idH

ighe

rH

ighe

rhLo

wer

Mid

Mid

Low

erM

idT

opt

~29°

Ce ;

slow

grow

erS

alty

envi

ronm

ents

;an

imal

and

plan

tsu

rfac

es

Into

lera

nce

tom

atric

stre

ss;

asl

ow-g

row

ing

halo

phile

Klu

yver

omyc

esm

arxi

anus

(CB

S71

2)H

ighe

rLo

wer

Mid

Low

erH

ighe

rM

idLo

wer

Hig

her

Low

erT

opt

~38–

40°C

;T

max

65°C

e ;no

tfa

st-g

row

ing

Milk

;pl

ant

surf

aces

;na

tura

lfer

men

tatio

nsT

herm

otol

eran

t,so

lute

-into

lera

ntan

dxe

ro-in

tole

rant

i

Pic

hia

(Kod

amae

a)oh

mer

i(U

WO

PS

05–2

28.2

)H

ighe

rM

idH

ighe

rH

ighe

rH

ighe

rH

ighe

rH

ighe

rH

ighe

rM

idT

opt

~33°

C;

Tm

ax>

50°C

e ;fa

st-

grow

erB

eetle

s;fr

uits

and

othe

rpl

ant

Mul

tiple

stre

ssto

lera

nces

incl

udin

get

hano

lan

dsu

gar;

stre

ssp

hen

oty

pe

of

axe

roto

lera

nt,

vig

oro

us

wee

dj

Pic

hia

(Kom

agat

aella

)pa

stor

is(C

BS

704)

Mid

Low

erLo

wer

Mid

Hig

her

Mid

Low

erH

ighe

rM

idpH

min

~2.2

e ;no

tfa

st-g

row

ing

Rot

ting

woo

d;sl

imes

Into

lera

ntto

osm

otic

stre

ss,

glyc

erol

and

suga

r;a

xero

-into

lera

ntye

ast

Pic

hia

sydo

wio

rum

(UW

OP

S03

–414

.2)

Hig

her

Mid

Hig

her

Hig

her

Hig

her

Hig

her

Mid

Hig

her

Hig

her

pHop

t~6

–8e ;

fast

grow

erP

ollu

ted

envi

ronm

ents

;w

aste

wat

erM

ultip

lest

ress

tole

ranc

esin

clud

ing

etha

nol

and

suga

r;st

ress

ph

eno

typ

eo

fa

xero

tole

ran

t,vi

go

rou

sw

eed

j

Rho

doto

rula

crea

tiniv

ora

(PB

7)Lo

wer

Low

erM

idM

idLo

wer

Low

erLo

wer

Mid

Hig

her

Top

t~1

0°C

;T

min

~1°C

e ;sl

owgr

ower

Sub

surf

ace;

soil

Into

lera

ntto

alco

hols

,gl

ycer

ol;

xero

tole

rant

aps

ychr

ophi

licsl

owgr

ower

Sac

char

omyc

odes

ludw

igii

(UW

OP

S92

–218

.4)

Low

erM

idH

ighe

rLo

wer

Low

erLo

wer

Low

erLo

wer

Low

erpH

min

~2e ;

slow

grow

erG

rape

s;pl

ant

tissu

esan

dfe

rmen

tatio

nsIn

tole

rant

togl

ycer

olan

dN

aCl;

tole

rant

tosu

gars

;an

osm

ophi

leZ

ygos

acch

arom

yces

roux

ii(C

BS

732)

Mid

Hig

her

Hig

her

Low

erM

ixed

Hig

her

Mid

Mid

Mid

pHop

t3–

7;pH

min

1.5–

2e ;sl

owgr

ower

Fru

itsan

dot

her

high

-sug

arha

bita

tsIn

tole

rant

toN

aCl;

tole

rant

togl

ycer

olan

dsu

gars

;an

osm

ophi

le

a.S

ourc

esof

stra

ins

are

give

nin

Fig

.2.

b.

Bas

edon

data

for

grow

thon

MY

PiA

at30

°C(s

eeF

ig.2

).A

lcoh

ols

wer

eet

hano

land

met

hano

l,su

gars

wer

efr

ucto

sean

dsu

cros

e,sa

ltsw

ere

NaC

l,M

gCl 2

and

amm

oniu

msu

lfate

,th

eot

her

stre

ssor

sw

ere

prol

ine,

xant

ham

gum

and

PE

G80

00(F

ig.2

).C

haot

rope

stre

ssis

indu

ced

byet

hano

l,fr

ucto

se,

glyc

erol

and

MgC

l 2;

osm

otic

stre

ssby

fruc

tose

,su

cros

e,N

aCla

ndpr

olin

e;m

atric

stre

ssby

xant

ham

gum

and

PE

G80

00;

and

kosm

otro

pest

ress

byam

mon

ium

sulfa

te(F

ig.2

;B

row

n,19

90;

Hal

lsw

orth

,19

98;

Hal

lsw

orth

etal

.,20

03a;

Hal

lsw

orth

etal

.,20

07;

Will

iam

san

dH

alls

wor

th,

2009

;B

haga

nna

etal

.,20

10;

Chi

net

al.,

2010

;C

ray

etal

.,20

13).

Str

ess-

tole

ranc

eas

sess

men

ts(h

ighe

r,m

id-r

ange

,lo

wer

)ar

ere

lativ

eto

the

rang

eof

thos

eof

the

othe

rsp

ecie

sas

saye

d,an

dba

sed

onva

lues

inF

ig.2

.c.

Tem

pera

ture

optim

a,m

inim

aan

d/or

max

ima

(Top

t,T

min

,T

max

)an

dpH

optim

a,m

inim

aan

d/or

max

ima

(pH

opt,

pHm

in,

pHm

ax)

for

grow

thw

ere

obta

ined

from

cite

dpu

blic

atio

ns.

Ext

rem

egr

owth

phen

otyp

es(f

ast

orsl

owgr

ower

s)w

ere

liste

dac

cord

ing

togr

owth

rate

son

MY

PiA

at30

°C(s

eeal

soF

ig.2

).S

peci

esde

sign

ated

assl

owgr

ower

sdi

dno

tha

vea

vigo

rous

grow

thph

enot

ype

unde

rth

ese

cond

ition

s;i.e

.al

lstr

ains

liste

dar

eab

leto

grow

rapi

dly

with

inth

eas

say

perio

don

/at

thei

rfa

vour

edm

edia

/tem

pera

ture

.T

hede

sign

atio

nsl

owgr

owin

gdi

dno

tre

late

toan

exte

nded

lag

phas

e(d

ata

not

show

n).

d.

Prim

arily

base

don

data

pres

ente

din

the

curr

entt

able

asw

ella

sF

ig.2

(unl

ess

othe

rwis

est

ated

)so

ism

ostp

ertin

entt

ohi

gh-s

ugar

habi

tats

at~3

0°C

.Hab

itatd

omin

ance

will

ultim

atel

ybe

influ

ence

dby

antim

icro

bial

activ

ities

ofsp

ecie

spr

esen

tw

ithin

aco

mm

unity

;se

eTa

ble

6).

Eco

phys

iolo

gica

ldes

crip

tions

ofw

eed-

like

spec

ies

are

unde

rline

din

bold

.e.

Val

ues

for

tem

pera

ture

-an

dpH

-tol

eran

ces

wer

eta

ken

from

:(f

orS

.cer

evis

iae)

Pra

phai

long

and

Fle

et(1

997)

,Y

alci

nan

dO

zbas

(200

8)an

dS

alva

dóan

dco

lleag

ues

(201

1);

(for

C.t

erre

us)

Kra

llish

and

colle

ague

s(2

006)

;(f

orD

.han

seni

i)D

omín

guez

and

colle

ague

s(1

997)

;(fo

rH

.pol

ymor

pha)

Levi

nean

dC

oone

y(1

973)

;(fo

rH

.wer

neck

ii)D

íaz

Muñ

ozan

dM

onta

lvo-

Rod

rígu

ez(2

005)

;(fo

rK

.mar

xian

us)A

ziz

and

colle

ague

s(2

009)

;Sal

vadó

and

colle

ague

s(2

011)

;(fo

rP.

ohm

eri)

Zhu

and

colle

ague

s(2

010)

;(f

orP.

past

oris

)C

hiru

volu

etal

.(1

998)

;(f

orP.

sydo

wio

rum

)K

anek

aran

dco

lleag

ues

(200

9);

(for

R.c

reat

iniv

ora)

Kra

llish

and

colle

ague

s(2

006)

;(f

orS

.lud

wig

ii)S

trat

ford

(200

6);

and

(for

Z.r

ouxi

i)R

esta

ino

and

colle

ague

s(1

983)

and

Pra

phai

long

and

Fle

et(1

997)

.To

lera

nce

win

dow

sfo

rC

andi

daet

chel

lsii

are

yet

tobe

esta

blis

hed.

f.U

nder

som

eco

nditi

ons

stra

ins

ofS

.cer

evis

iae

can

tole

rate

upto

28%

v/v

(20%

w/v

)et

hano

l(se

eH

alls

wor

th,

1998

).g

.S

eeal

soK

ralli

shan

dco

lleag

ues

(200

6).

h.

Inhi

gh-s

alt

habi

tats

,H

.wer

neck

iica

ngr

owat

mol

arco

ncen

trat

ions

ofN

aCl(

see

Gun

de-C

imer

man

etal

.,20

00)

but

was

less

salt

tole

rant

unde

rth

eco

nditi

ons

ofth

isas

say.

i.T

his

spec

ies

appe

ars

toha

vea

requ

irem

ent

for

high

wat

erac

tivity

.j.

Hab

itatd

omin

ance

can

also

depe

ndon

fact

ors

such

aspr

oduc

tion

ofan

timic

robi

als

(see

also

Tabl

e6)

.Pic

hia

ohm

eric

ando

min

ate

som

eha

bita

ts,P

ichi

aan

omal

am

aybe

mor

evi

goro

usas

aw

eed

spec

ies

(see

Ros

aet

al.,

1990

;Lee

etal

.,20

11).



protein-stabilizing proteins, metabolic enzymes andcellular-organization proteins are regulated by a singlepromoter – the stress response element (STRE) – whichis activated under cellular stress. This regulatory systemenables the coordination of an array of stress responsesin an energy-efficient manner (Table 3). Numerousstudies show that the S. cerevisiae responses to osmoticstress [via the high-osmolarity glycerol-response (HOG)pathway], oxidative stress, and challenges to protein andmembrane stability are exceptionally efficient (Table 3;Brown, 1990; Costa et al., 1997; Hallsworth, 1998;Rodríguez-Peña et al., 2010; Szopinska and Morsomme,2010). In addition to these stress responses, there isevidence that the dynamics of polyphosphate and glyco-gen metabolism in S. cerevisiae are wired in such a wayto boost ATP production (Castrol et al., 1999), and that theploidy levels of many strains enhance tolerance towardsoxidative and other stresses (Table 3). The energy-generation and energy-conservation strategies employedby S. cerevisiae have apparent parallels in other weedspecies; for example, analyses of synonymous codonbias in the genomes of fast-growing bacteria includingE. coli and Bacillus subtilis suggest that genes associatedwith energy generation are highly expressed (Karlin et al.,2001; Table 5; see also above). The enhanced energyefficiency that is apparent in some weed species not onlyunderpins their robust stress biology, but is required tosustain a vigorous growth phenotype and/or to out-growcompetitors.

Growth, nutritional versatility, and resource acquisitionand storage

Efficient cell division and an ability to out-grow competi-tors are implicit to the emergence of weed species.Species that grow relatively slowly or remain quiescent,and those with specific requirements for a host, a sym-biotic partner, or obligate interactions with other microbialspecies are disadvantaged during community develop-ment in open habitats: dominance ultimately results fromvigour and – in many habitats – a degree of nutritionalversatility (Tables S1 and 5). Ability to out-grow competi-tors is equally important (possibly even more so) forweed species in nutrient-poor and physicochemicallyextreme habitats that can both select for slow-growingspecies and limit overall biomass development. Manytraits that give rise to an efficient growth phenotype canbe found in weed species (Table 5): multiple copies ofribosomal DNA operons that can enhance rates ofprotein synthesis; transport proteins to scavenge macro-molecules thus negating the need for de novo synthesis;high-efficiency DNA polymerase for rapid genome repli-cation; efficient systems to eliminate reactive oxygenspecies that are a by-product of rapid growth; and poly-

ploidy, aneuploidy and plasmids that can be associatedwith enhanced stress tolerance, higher growth-rates andincreased overall vigour (Table 5). We believe thatanother key aspect of weed biology for some microbialspecies is their ability to sequester and store availablenutrient and substrate molecules with a high efficiency asan auxiliary energy reserve (see below), to be able tosupply daughter cells with nutrients, and simultaneouslydeprive other microbes of nutritional resources (e.g. Duiffet al., 1993; Castrol et al., 1999; Loaces et al., 2011;Renshaw et al., 2002; Jahid et al., 2006). Microbialweeds are highly efficient at nutrient-sequestration andsubstrate utilization, as well as intracellular storage ofthese substances (Table 5). For example, fungalsiderophores that remove iron from the habitat havebeen shown to suppress growth of other microorganismsdue to iron limitation (Renshaw et al., 2002).

Intermittent nutrient availability and low nutrient con-centrations are characteristic of many aquatic environ-ments so the ability to scavenge and store, circumventthe requirement for, or strategically utilize scarce andpotentially limiting nutrients can greatly enhance thecompetitive ability of planktonic species. Underphosphate-limiting conditions some aquatic species,including S. ruber, are able to use sulfur-containing gly-colipids in place of phospholipids during low phosphateavailability (Table 5). The cyanobacterium M. aeruginosahas high-efficiency phosphate-transport systems andaccumulates intracellular polyphosphate which is used tomaintain activity once extracellular phosphate is depleted(Table 5; Shi et al., 2003). It is likely that this trait con-tributes to its weed-like phenotype in Lake Taihu (China)that is a well-studied, phosphate-limited habitat fre-quently dominated by M. aeruginosa (Shi et al., 2003).Iron is another potentially limiting nutrient in aquatic habi-tats. Dunaliella salina utilizes a highly efficient iron-binding protein to take up iron which is then stored invacuoles (Paz et al., 2007). Species such as D. salinaand H. walsbyi cope with oligotrophic conditions byhyperaccumulating starch and/or lipids such as polyhy-droxybutyrate especially when nutrients other thancarbon are limiting (Table 5; Bardavid et al., 2008). Oneweed species with adaptations to endure low-nitrogenconditions is Mycobacterium smegmatis. This species(as well as other mycobacteria) which can be prevalentin relatively low-nutrient aquatic and non-aquatic habitats(Koch, 2001; Kazda and Falkinham III, 2009) have bio-chemical adaptations to enable growth and metabolicactivity even when nitrogen concentrations are an orderof magnitude lower than those usually required for struc-tural growth (i.e. a C : N ratio of 8:1; Roels, 1983;Behrends et al., 2012). In addition to nitrogen oligotro-phy, M. smegmatis has a DNA polymerase capable ofnucleotide processing rates and generation times that



Tab

le5.

Gro

wth

,nu

triti

onal

vers

atili

tyan

dre

sour

ceac

quis

ition

and

stor

age:

cellu

lar

char

acte

ristic

sth

atco

ntrib

ute

tow

eed-

like

beha

viou

r.a

Met

abol

ites,

prot

eins

,m

olec

ular

char

acte

ristic

s,an

dot

her

trai

tsF

unct

ion(

s)P

heno

typi

ctr

aits

Not

esan

dre

fere

nces

Ab

ility

too

ut-

gro

wco

mp

etit

ors

Mul

tiple

copi

esof

ribos

omal

DN

Aop

eron

sE

nhan

ced

prod

uctio

nof

ribos

omes

Rap

idpr

otei

nsy

nthe

sis

Soi

lbac

teria

able

togr

owra

pidl

yon

high

-nut

rient

med

iaha

vean

aver

age

of~

5.5

copi

esof

ribos

omal

DN

Aop

eron

s(c

ompa

red

with

~1.

4co

pies

for

slow

-gro

win

gsp

ecie

s;K

lapp

enba

chet

al.,

2000

)K

eyro

les

ofdi

-/tr

ipep

tide-

tran

spor

tpr

otei

n(d

tpT

)an

dol

igop

eptid

etr

ansp

ort

AT

P-b

indi

ngpr

otei

n(O

pp)

Per

mea

se(d

tpT

)an

dA

BC

-typ

etr

ansp

orte

r(O

pp)

that

enab

leef

ficie

ntsc

aven

ging

ofdi

vers

epe

ptid

es(A

lterm

ann

etal

.,20

05)

Effi

cien

tup

take

ofdi

vers

epe

ptid

esT

hese

prot

eins

enab

lesp

ecie

ssu

chas

Lact

obac

illus

acid

ophi

lus

toef

ficie

ntly

scav

enge

pept

ides

and

ther

eby

min

imiz

eth

ene

edfo

rde

novo

synt

hesi

sof

amin

oac

ids

(Alte

rman

net

al.,

2005

)

Hig

h-ef

ficie

ncy

DN

Apo

lym

eras

eA

ppar

ent

corr

elat

ion

with

shor

tge

nera

tion-

time

infa

st-g

row

ing

bact

eria

(Cou

turie

ran

dR

ocha

,20

06)

Rap

idge

nom

ere

plic

atio

nT

here

lativ

ely

fast

-gro

win

gM

ycob

acte

rium

smeg

mat

is(g

ener

atio

ntim

e~

3h)

has

aD

NA

poly

mer

ase

proc

essi

ngra

teof

600

nucl

eotid

es-1

,co

mpa

red

with

50nu

cleo

tide

s-1fo

rM

ycob

acte

rium

tube

rcul

osis

(gen

erat

ion

time

~24

h;S

trau

san

dW

u,19

80;

Cou

turie

ran

dR

ocha

,20

06)

Ove

rlapp

ing

repl

icat

ion

cycl

esB

acte

riaca

nin

itiat

ea

new

roun

dof

chro

mos

omal

DN

Are

plic

atio

nbe

fore

the

com

plet

ion

ofan

ongo

ing

roun

dof

synt

hesi

s

Rap

idge

nom

ere

plic

atio

nE

sche

richi

aco

lica

nop

erat

eup

toei

ght

orig

ins

ofre

plic

atio

nsi

mul

tane

ousl

y(s

eeN

ords

tröm

and

Das

gupt

a,20

06)

Pol

yplo

idy,

aneu

ploi

dy,

asso

ciat

ion

with

plas

mid

s,an

d/or

hybr

idiz

atio

nth

aten

hanc

e(s)

vigo

ur

Mul

tiple

copi

esof

geno

mic

DN

Aca

nle

adto

incr

ease

dvi

talit

y,en

hanc

edgr

owth

rate

s,in

crea

sed

prod

uctio

nof

antim

icro

bial

s,an

den

hanc

eden

ergy

gene

ratio

nan

dst

ress

tole

ranc

e(s

eeal

soTa

ble

3)

Enh

ance

dvi

gour

Sho

rter

gene

ratio

ntim

esin

poly

ploi

dba

cter

iam

ayar

ise

from

anu

mbe

rof

fact

ors

incl

udin

gth

ein

crea

sed

num

ber

ofrib

osom

alD

NA

oper

ons

(Cox

,20

04;

see

also

abov

e)an

dge

nelo

caliz

atio

nw

ithin

the

geno

me

(Pec

orar

oet

al.,

2011

).A

rece

ntst

udy

ofF

1hy

brid

spr

oduc

edby

cros

sing

16w

ild-t

ype

stra

ins

ofS

.cer

evis

iae

show

edth

atm

any

F1

stra

ins

disp

laye

dhy

brid

vigo

ur(T

imbe

rlake

etal

.,20

11)b

Trai

tsfo

rhi

gh-e

ffici

ency

ener

gyge

nera

tion

(see

Tabl

e3)

Effi

cien

tsy

stem

toel

imin

ate

free

radi

cals

(see

also

Tabl

e3)

Elim

inat

ion

ofre

activ

eox

ygen

spec

ies

that

can

reac

tw

ithan

dda

mag

em

acro

mol

ecul

aran

dce

llula

rst

ruct

ures

Abi

lity

toco

pew

ithth

eox

idat

ive

stre

ssas

soci

ated

with

high

grow

thra

tes

The

enha

nced

rate

sof

oxid

ativ

eph

osph

oryl

atio

nre

quire

dfo

rra

pid

grow

thre

sult

inth

ein

crea

sed

gene

ratio

nof

free

radi

cals

;a

phen

omen

onth

atha

sbe

enob

serv

edin

plan

tw

eeds

(Wu

etal

.,20

11).

Asp

ergi

llus

mut

ants

that

lack

supe

roxi

dedi

smut

ase

gene

sar

eun

able

togr

owun

der

envi

ronm

enta

lcon

ditio

nsth

atfa

vour

ahi

ghm

etab

olic

rate

(Lam

bou

etal

.,20

10).

Str

ains

ofP

seud

omon

asae

rugi

nosa

have

anau

xilia

rym

anga

nese

-dep

ende

ntve

rsio

nof

supe

roxi

dedi

smut

ase

that

does

not

requ

ireiro

nan

dis

upre

gula

ted

unde

riro

n-lim

iting

cond

ition

s(B

ritig

anet

al.,

2001

)N

utr

itio

nal

and

met

abo

licve

rsat

ility

c

Gen

esfo

rca

tabo

lism

ofa

wid

esp

ectr

umof

hydr

ocar

bons

;e.

g.th

ose

codi

ngfo

rth

eca

tech

ol-,

hom

ogen

tisat

e-,

phen

ylac

etat

e-an

dpr

otoc

atec

huat

e-ca

tabo

licpa

thw

ays

(cat

,hm

g,ph

aan

dpc

age

nefa

mili

esre

spec

tivel

y)

Fac

ilita

teth

esy

nthe

sis

ofpr

otei

nsth

aten

able

the

utili

zatio

nof

hydr

ocar

bons

(incl

udin

gpo

lycy

clic

arom

atic

hydr

ocar

bons

)

Abi

lity

tout

ilize

dive

rse

hydr

ocar

bons

asa

carb

onan

d/or

ener

gyso

urce

Suc

hco

mpo

unds

can

beut

ilize

das

aso

leca

rbon

sour

ceby

asm

alln

umbe

rof

met

abol

ical

lyve

rsat

ilem

icro

bes

such

asP

anto

easp

p.,

Pse

udom

onas

putid

aan

dP

ichi

aan

omal

a(T

imm

is,

2002

;P

anet

al.,

2004

;V

asile

va-T

onko

vaan

dG

eshe

va,

2007

)bu

tar

eal

sokn

own

toex

ert

cellu

lar

stre

ssev

enat

low

conc

entr

atio

ns(B

haga

nna

etal

.,20

10).

Cat

abol

ism

ofhy

droc

arbo

nsw

illth

eref

ore

alle

viat

est

ress

atth

esa

me

time

aspr

ovid

ing

for

ener

gyge

nera

tion

and

grow

th(J

imén

ezet

al.,

2002

;D

omín

guez

-Cue

vas

etal

.,20

06)

Cat

abol

ite-r

epre

ssio

nsy

stem

for

ener

gy-e

ffici

ent

utili

zatio

nof

com

plex

subs

trat

es

Adv

ance

dsy

stem

tore

gula

teut

iliza

tion

ofdi

vers

esu

bstr

ates

Ene

rgy-

effic

ient

grow

thin

nutr

ition

ally

com

plex

envi

ronm

ents

AcA

MP

-inde

pend

ent

cata

bolit

e-re

pres

sion

syst

emha

sbe

enid

entifi

edin

P.pu

tida

that

enab

les

the

orde

red

assi

mila

tion

ofca

rbon

,ni

trog

enan

dsu

lfur

subs

trat

es(m

ost

ener

gy-f

avou

rabl

efir

st;

Dan

iels

etal

.,20

10)

Pro

duct

ion

and

secr

etio

nof

bios

urfa

ctan

ts(e

.g.

rham

nolip

ids

inP

anto

ea,

P.ae

rugi

nosa

and

P.pu

tida;

glyc

olip

opro

tein

sin

Asp

ergi

llus

spp.

)

Sol

ubili

zatio

nof

hydr

opho

bic

mol

ecul

es(a

ndan

timic

robi

alac

tivity

;se

eTa

ble

6)A

bilit

yto

enha

nce

the

bioa

vaila

bilit

yof

hydr

opho

bic

subs

trat

es

Invi

tro

stud

ies

ofP

anto

eaan

dP.

aeru

gino

sade

mon

stra

teth

atbi

osur

fact

ants

enha

nce

the

upta

keof

hydr

opho

bic

subs

trat

es(A

l-Tah

han

etal

.,20

00;

Vas

ileva

-Ton

kova

and

Ges

heva

,20

07;

Rei

set

al.,

2011

)an

dth

ereb

yfa

cilit

ate

colo

niza

tion

ofhy

droc

arbo

n-co

ntai

ning

habi

tats

(see

Tabl

eS

1).

Asp

ergi

llus

spec

ies

can

prod

uce

copi

ous

amou

nts

ofbi

osur

fact

ant

(Des

aian

dB

anat

,19

97;

Kira

net

al.,

2009

)D

iver

sesa

prot

roph

icen

zym

es(e

.g.

cellu

lose

,lig

nina

se)

able

tofu

nctio

nov

era

rang

eof

cond

ition

s

Ext

race

llula

rde

grad

atio

nof

poly

mer

icor

gani

cm

olec

ules

for

use

asa

carb

onan

den

ergy

sour

ceA

bilit

yto

grow

sapr

otro

phic

ally

Sap

rotr

ophi

cca

pabi

litie

sen

hanc

eth

era

nge

ofsu

bstr

ates

from

whi

chnu

triti

onca

nbe

obta

ined

.S

apro

trop

hic

enzy

mes

from

Asp

ergi

llus

spec

ies

can

func

tion

over

aw

ide

rang

eof

envi

ronm

enta

lstr

esse

s(H

ong

etal

.,20

01)

Pro

tein

sfo

rox

idat

ion

ofm

etha

nean

d/or

met

hano

l(e.

g.al

coho

loxi

dase

inP

ichi

aan

dK

odam

aea)

Oxi

datio

nof

one-

carb

onsu

bstr

ates

that

are

used

for

ener

gyge

nera

tion/

grow

thA

bilit

yto

utili

zeon

e-ca

rbon

subs

trat

esO

ne-c

arbo

nsu

bstr

ates

are

envi

ronm

enta

llyco

mm

onpl

ace

and

thei

rut

iliza

tion

can

faci

litat

era

pid

grow

th(v

ande

rK

leie

tal.,

1991

;M

cDon

ald

and

Mur

rell,

1997

;P

ache

coet

al.,

2003

)

Pat

hway

sto

utili

zea

broa

dra

nge

ofni

trog

ensu

bstr

ates

(e.g

.D

-am

ino

acid

s,ur

ea,

amm

oniu

msa

lts,

and

mac

rom

olec

ules

such

asco

llage

nan

del

astin

)

Ass

imila

tion

ofni

trog

enin

toan

abol

icpa

thw

ays

for

deno

vosy

nthe

sis

ofam

ino

acid

san

dnu

clei

cac

ids

Abi

lity

tout

ilize

aw

ide

spec

trum

ofni

trog

enso

urce

s

Ver

satil

ityin

the

utili

zatio

nof

nitr

ogen

subs

trat

esca

nen

able

prol

ifera

tion

inop

enha

bita

tsby

,an

dop

port

unis

ticpa

thog

enic

ityfo

r,A

sper

gillu

s,P

seud

omon

aspu

tida

and

othe

rw

eed

spec

ies

(Kra

ppm

ann

and

Bra

us,

2005

;D

anie

lset

al.,

2010

;se

eal

soTa

ble

S1)

.R

hodo

toru

lasp

p.,

incl

udin

gm

etab

olic

ally

vers

atile

wee

dsp

ecie

s,ca

ngr

owon

D-a

min

oac

ids

asa

sole

carb

onan

dni

trog

enso

urce

(Sim

onet

taet

al.,

1989

;P

olle

gion

ieta

l.,20

07)

Gen

ome-

med

iate

dre

spon

ses

tom

aint

ain

grow

thun

der

low

-nut

rient

cond

ition

s(e

.g.

upre

gula

tion

ofgl

utam

ate

dehy

drog

enas

ein

P.pu

tida)

Glu

tam

ate

dehy

drog

enas

epl

ays

key

role

sin

nitr

ogen

assi

mila

tion

and

met

abol

ism

Abi

lity

toad

apt

met

abol

ism

for

grow

that

high

-or

low

-nut

rient

conc

entr

atio

ns

Exp

ress

ion

ofgd

hw

asbe

twee

n5-

and

26-f

old

grea

ter

inP.

putid

ace

llsun

der

low

-nut

rient

cond

ition

sco

mpa

red

with

ahi

gh-n

utrie

ntco

ntro

l(S

ynet

al.,

2004

).T

hesy

nthe

sis

ofgl

utam

ate

via

glut

amat

ede

hydr

ogen

ase,

rath

erth

angl

utam

ate

synt

hase

,co

nsum

es20

%le

ssA

TP

(Syn

etal

.,20

04)



Enz

yme

syst

ems

that

enab

lem

etab

olis

mun

der

nutr

ient

-lim

iting

cond

ition

sby

avoi

ding

depe

nden

ceon

spec

ific

cofa

ctor

s

Util

izat

ion

ofsu

bstit

ute

cofa

ctor

,or

repl

acem

ent

ofen

zym

esy

stem

(s)

that

wou

ldre

quire

aco

fact

orth

atis

envi

ronm

enta

llysc

arce

Mai

nten

ance

ofes

sent

ial

enzy

me

func

tions

atlo

wnu

trie

ntco

ncen

trat

ions

For

exam

ple

argi

nase

inS

.cer

evis

iae

(Mid

delh

oven

etal

.,19

69)

and

phos

phol

ipas

eC

inP.

aeru

gino

sa(S

tinso

nan

dH

ayde

n,19

79)

Pat

hway

sto

synt

hesi

zeph

osph

ate-

free

mem

bran

elip

ids

Mai

nten

ance

ofm

embr

ane

func

tions

unde

rph

osph

ate-

limite

dco

nditi

ons

Abi

lity

tore

mai

nac

tive,

and

grow

,in

phos

phat

e-de

plet

eden

viro

nmen

ts

Pse

udom

onas

spp.

can

synt

hesi

zem

embr

anou

sgl

ycol

ipid

sas

anal

tern

ativ

eto

phos

phol

ipid

sun

der

low

-pho

spha

teco

nditi

ons

(Min

niki

net

al.,

1974

).S

alin

ibac

ter

rube

ran

da

num

ber

ofph

ytop

lank

ton

spec

ies

utili

zesu

lfur

inm

embr

ane

glyc

olip

ids

that

have

asu

lfoqu

inov

ose-

cont

aini

ng(n

on-p

hosp

horu

s)he

adgr

oup

and

are

synt

hesi

zed

inre

spon

seto

low

phos

phat

eav

aila

bilit

y(B

enni

ng,

1998

;C

orce

lliet

al.,

2004

;B

ellin

ger

and

Van

Moo

y,20

12)

Hig

hgl

ucos

ylgl

ycer

ate

unde

rlo

w-n

itrog

enco

nditi

ons

Con

trol

ofni

trog

enho

meo

stas

isto

enab

legr

owth

unde

rni

trog

en-li

miti

ngco

nditi

ons

Nitr

ogen

olig

otro

phy

Intr

acel

lula

rgl

ucos

ylgl

ycer

ate

isin

crea

sed

inM

.sm

egm

atis

unde

rlo

wni

trog

enco

nditi

ons.

Mut

ants

unab

leto

synt

hesi

zegl

ucos

ylgl

ycer

ate

show

edre

duce

dup

take

ofam

mon

ium

and

are

duce

dgr

owth

rate

(Beh

rend

set

al.,

2012

)

Eff

icie

nt

acq

uis

itio

nan

dst

ora

ge

of

reso

urc

esTr

ansp

ort

prot

eins

tosc

aven

gepe

ptid

esan

d/or

othe

rm

acro

mol

ecul

esE

ffici

ent

scav

engi

ngof

biom

acro

mol

ecul

esav

oidi

ngth

ene

edfo

rde

novo

synt

hesi

sE

ffici

ent

upta

keof

subs

trat

esF

orex

ampl

ein

L.ac

idop

hilu

s(s

eeal

soab

ove;

Alte

rman

net

al.,

2005

)

Bio

surf

acta

nts

toac

cess

hydr

opho

bic

subs

trat

es(s

eeab

ove)

Pro

duct

ion

ofhi

ghqu

antit

ies

ofhi

gh-

affin

itysa

prop

trop

hic

enzy

mes

Effi

cien

tde

grad

atio

nof

com

plex

extr

acel

lula

rsu

bsta

nces

Effi

cien

tut

iliza

tion

ofhi

gh-M

r

subs

trat

esF

orex

ampl

e.xy

lana

ses

prod

uced

byA

cine

toba

cter

juni

iand

Asp

ergi

llus

spp.

(Mea

gher

etal

.,19

88;

Loet

al.,

2010

)H

igh-

affin

ityhe

xose

-tra

nspo

rtpr

otei

ns,

e.g.

Hxt

2p(H

XT

gene

fam

ily)

Hig

hly

effic

ient

upta

keof

dive

rse

carb

onsu

bstr

ates

Rap

idup

take

ofhe

xose

suga

rsT

hese

prot

eins

are

upre

gula

ted

inS

.cer

evis

iae

atlo

wsu

gar

conc

entr

atio

ns(W

ende

llan

dB

isso

n,19

94)

Phy

tase

,in

orga

nic

phos

phat

etr

ansp

ort

prot

eins

and

poly

phos

phat

eki

nase

Ext

race

llula

rde

grad

atio

nof

orga

nic

phos

phat

ean

dup

take

and

intr

acel

lula

rpo

lym

eriz

atio

nof

inor

gani

cph

osph

ate

Seq

uest

ratio

nan

dst

orag

eof

inor

gani

cph

osph

ate

Pic

hia

kudr

iavz

evii

has

ahi

ghra

teof

inor

gani

cph

osph

ate

prod

uctio

nfr

omph

ytat

e(H

ells

tröm

etal

.,20

12).

Red

uced

surv

ival

ofpo

lyph

osph

ate

kina

se-d

efici

ent

bact

eria

lmut

ants

has

been

obse

rved

atlo

wpH

,hi

ghsa

linity

,an

dun

der

oxid

ativ

est

ress

(Jah

idet

al.,

2006

).O

ther

wee

dsp

ecie

s,su

chas

P.pu

tida,

Dun

alie

llasa

lina,

Mic

rocy

stis

aeru

gino

saan

dO

stre

ococ

cus

taur

iare

effic

ient

accu

mul

ator

sof

poly

phos

phat

e(B

enta

leta

l.,19

91;

Shi

etal

.,20

03;

Tobi

net

al.,

1997

;20

07;

LeB

ihan

etal

.,20

11)

Pro

duct

ion

and

secr

etio

nof

side

roph

ores

that

chel

ate

iron

Tosc

aven

geiro

nfr

omth

eex

trac

ellu

lar

mili

euw

hich

isth

enre

mov

edon

ceth

esi

dero

phor

esha

vebe

entr

ansp

orte

dba

ckin

toth

ece

ll

Effi

cien

tsc

aven

ging

ofiro

nT

heco

mpe

titiv

eab

ility

ofso

me

bact

eria

lwee

ds(e

.g.

pseu

dom

onad

s,P

anto

eaan

anat

is)

may

been

hanc

edby

side

roph

ore

prod

uctio

n(D

uiff

etal

.,19

93;

Loac

eset

al.,

2011

).R

hodo

toru

lam

ucila

gino

saan

dM

.aer

ugin

osa

upre

gula

tesi

dero

phor

epr

oduc

tion

unde

riro

n-lim

iting

cond

ition

s(A

nder

sen

etal

.,20

03;

Xin

get

al.,

2007

);in

cont

rast

,S

acch

arom

yces

spp.

are

not

know

nto

prod

uce

side

roph

ores

(Les

uiss

eet

al.,

2001

)E

nhan

ced

effic

ienc

yof

iron-

bind

ing

prot

eins

(e.g

.tr

ansf

errin

-like

prot

ein,

TT

f,in

D.s

alin

a)

Bin

ding

and

upta

keof

extr

acel

lula

riro

nA

bilit

yto

accu

mul

ate

iron

unde

riro

n-lim

iting

cond

ition

sD

unal

iella

salin

ace

llsun

derg

oa

four

fold

incr

ease

iniro

n-bi

ndin

gaf

finity

unde

rlo

w-ir

onco

nditi

ons.

Iron

isth

enta

ken

upst

ored

inva

cuol

es(P

azet

al.,

2007

)

Arg

inin

ebi

osyn

thes

ispr

otei

nsB

ulk

synt

hesi

sof

argi

nine

asa

nitr

ogen

subs

trat

est

ore

Am

ino

acid

accu

mul

atio

nan

dst

orag

eS

acch

arom

yces

cere

visi

aest

ores

argi

nine

(inva

cuol

es)

that

can

beut

ilize

dw

hen

the

extr

acel

lula

ren

viro

nmen

tbe

com

esni

trog

ensu

bstr

ate

limite

d(W

este

nber

get

al.,

1989

)Tr

ehal

ose-

synt

hesi

spr

otei

ns(e

.g.

TP

S,

TP

P)

and

glyc

ogen

synt

hase

(e.g

.G

SY

1an

dG

SY

2)

Syn

thes

isof

disa

ccha

ride-

and

poly

sacc

harid

e-st

orag

eco

mpo

unds

(e.g

.tr

ehal

ose

and

glyc

ogen

resp

ectiv

ely)

Effe

ctiv

esy

nthe

sis

and

stor

age

ofca

rboh

ydra

tes

Treh

alos

esy

nthe

sis

can

beup

regu

late

dpr

ior

toth

est

atio

nary

grow

thph

ase

and

durin

gst

ress

(Par

rou

etal

.,19

97),

and

glyc

ogen

synt

hesi

sis

upre

gula

ted

durin

gpe

riods

ofnu

trie

ntlim

itatio

n,in

S.c

erev

isia

e(L

illie

and

Prin

gle,

1980

;F

arka

set

al.,

1990

).S

tarc

his

accu

mul

ated

byD

.sal

ina

(Sto

ynov

a-B

akal

ova

and

Tonc

heva

-Pan

ova,

2003

)P

olyh

ydro

xybu

tyra

te-s

ynth

esis

prot

eins

(and

thos

epr

oduc

ing

othe

rst

orag

elip

ids)

Syn

thes

isof

lipid

stor

es(s

eeal

soTa

ble

3)B

ulk

stor

age

oflip

ids

Pol

yhyd

roxy

buty

rate

,in

the

form

ofin

trac

ellu

lar

gran

ules

,do

min

ates

the

cyto

plas

mof

Hal

oqua

drat

umw

alsb

yi(S

apon

etti

etal

.,20

11);

Dun

alie

llasp

p.al

sost

ore

lipid

s(C

hen

etal

.,20

11);

rece

ntst

udie

sof

P.pu

tida

sugg

est

that

carb

onan

den

ergy

can

bech

anne

lled

into

stor

age

ofpo

lyhy

drox

ybut

yrat

ew

ithou

ta

redu

ctio

nof

grow

thra

te(E

scap

aet

al.,

2012

)M

orph

olog

ical

and

phys

iolo

gica

lada

ptat

ions

toop

timiz

elig

htca

ptur

ean

dab

sorp

tion

ofox

ygen

and

nutr

ient

s

Fla

tce

llsh

ape

give

sa

high

surf

ace-

to-v

olum

era

tio;

gas

vesi

cles

help

tom

aint

ain

the

horiz

onta

lor

ient

atio

nof

plan

kton

icce

lls

Opt

imiz

edlig

htca

ptur

e,an

dox

ygen

and

nutr

ient

abso

rptio

n

The

rem

arka

ble

mor

phol

ogy

ofH

.wal

sbyi

cells

optim

izes

acqu

isiti

onof

reso

urce

sin

high

lyco

mpe

titiv

ehi

gh-s

alt

habi

tats

(Bol

huis

etal

.,20

06;

Bar

davi

det

al.,

2008

)

Effi

cien

tch

loro

phyl

laan

dch

loro

plas

tar

rang

emen

tO

ptim

izat

ion

oflig

htha

rves

ting

and

high

phot

osyn

thet

icra

teH

igh

phot

osyn

thet

icra

teH

abita

tdo

min

ance

byG

onyo

stom

umse

men

can

beat

trib

uted

,in

part

,to

havi

nga

high

erph

otos

ynth

etic

rate

than

othe

rau

totr

ophi

csp

ecie

s(C

olem

anan

dH

eyw

ood,

1981

;P

elto

maa

and

Oja

la,

2010

)G

enes

rela

ted

toga

ssy

nthe

sis

and

gas

vesi

cle

form

atio

n(e

.g.

gvp

fam

ilyin

M.a

erug

inos

a)

Gas

vesi

cles

prov

ide

buoy

ancy

toop

timiz

eac

cess

tolig

htan

dhi

ghox

ygen

conc

entr

atio

ns(c

lose

toth

ew

ater

:atm

osph

ere

inte

rfac

eof

aqua

ticha

bita

ts)

Abi

lity

toac

cess

reso

urce

sre

quire

dfo

rph

otos

ynth

esis

Twel

vege

nes

invo

lved

inga

ssy

nthe

sis

and

stor

age

have

been

iden

tified

inM

.aer

ugin

osa

(Mlo

uka

etal

.,20

04);

mod

els

sugg

est

regu

latio

nof

buoy

ancy

inM

.ae

rugi

nosa

has

ake

yro

lein

habi

tat

dom

inan

ce(B

onne

tan

dP

oulin

,20

02)

a.T

hecu

rren

ttab

lepr

ovid

esex

ampl

esof

prot

eins

,gen

esor

othe

rch

arac

teris

tics

that

can

beas

soci

ated

with

and

give

rise

tow

eedi

ness

;the

cate

gorie

sof

trai

tsar

eno

tmut

ually

excl

usiv

e.In

divi

dual

trai

tsm

ayno

tbe

uniq

ueto

mic

robi

alw

eeds

;ho

wev

er,

wee

dssp

ecie

sar

elik

ely

toha

vea

num

ber

ofth

ese

type

sof

char

acte

ristic

s.b

.W

here

aspo

lypl

oidy

can

enha

nce

vigo

ur(v

iain

crea

sed

grow

thra

tes,

enha

nced

stre

ssto

lera

nce

etc.

)in

crea

sed

chro

mos

ome

num

ber

can

also

resu

ltin

decr

ease

dgr

owth

rate

s;th

eco

nseq

uenc

esof

poly

ploi

dyca

nva

ryw

ithsp

ecie

san

den

viro

nmen

talc

onte

xt.

c.N

utrit

iona

lver

satil

ityis

part

icul

arly

adva

ntag

eous

for

mic

robi

alw

eed

spec

ies

that

have

age

nera

list

lifes

tyle

such

asP

seud

omon

aspu

tida

and

Pic

hia

anom

ala

(Tim

mis

,20

02;

Wal

ker,

2011

).



are an order of magnitude faster than those of compa-rable Mycobacterium species (Table 5). Light and/oroxygen are key resources for many planktonic species;12 genes have been identified that are involved in gassynthesis and storage in species such as M. aeruginosaand H. walsbyi (Table 5). Modelling approaches indicatethat buoyancy, which enables the cell to access theupper (well-illuminated, well-oxygenated) section of thewater column, plays a key role in habitat dominance byM. aeruginosa (Bonnet and Poulin, 2002). Studies ofH. walsbyi suggest that its peculiar, flat cell-shape opti-mizes the uptake of nutrients and oxygen and its intrac-ellular gas vesicles help to maintain a horizontalorientation to capture light (Table 5). In freshwater habi-tats dominance of algal blooms by G. semen has beenattributed in part to a high photosynthetic rate that resultsfrom a combination of its high-efficiency chlorophyll aand a highly efficient chloroplast arrangement (Table 5).

In open habitats that are nutritionally dynamic and/orcomplex (Table S1) metabolic versatility in nutrient utiliza-tion can enhance the competitive ability of microbes (forexamples see Table 5). Pseudomonas putida and relatedspecies are remarkable in their range of nutritional strat-egies (Table 5; Timmis, 2002; 2009): they are able tocatabolize an indeterminate number of hydrocarbons (e.g.decanoate, toluene) and other organic molecules (e.g.amino acids, and organic acids such as acetic, citric andlactic acid) for use as carbon and energy sources; aminoacids, dipeptides, ammonium chloride, urea, ammoniumnitrate, and other substances as nitrogen sources; aminoacids, organic acids, sodium sulfite, thiouracil, agmatinesulfate, etc. as sulfur sources; as well as accumulatingdiverse substances as intracellular reserves (Chakrabartyand Roy, 1964; Daniels et al., 2010; Table 5) enabling aswitch to oligotrophic growth at low nutrient concentration(Table 5; Timmis, 2002). In addition, P. putida and closelyrelated species have evolved a complex, cAMP-independent catabolite repression system which incorpo-rates five different signals and enables an orderedassimilation of carbon, nitrogen and sulfur substrates fromthe most to least energetically favourable (Daniels et al.,2010). This may contribute to the ability of many pseu-domonads to sustain vigorous growth in nutritionallycomplex habitats. Pseudomonads, and closely relatedbacteria such as Acinetobacter, are not only environmen-tally ubiquitous but can dominate microbial communitiesin numerous types of open habitat including the plantphyllosphere and rhizosphere, bioaerosols, oil sands,and other hydrocarbon-containing environments (seeTable S1; Ogino et al., 2001; Röling et al., 2004; Louvelet al., 2011). Pseudomonas species are able to enhancethe availability of hydrophobic substrates by secretingbiosurfactants and, at the same time, tolerate the stressinduced by the latter (see below). Despite their copio-

trophic phenotype, pseudomonads utilize a number ofstrategies to maintain growth and metabolism underphosphate-, iron- or nitrogen-depleted conditions(Table 5), can synthesize glutamate via glutamate dehy-drogenase rather than glutamate synthase (thereby con-suming 20% less ATP; Syn et al., 2004), and have evenbeen observed growing in distilled water (Favero et al.,1971; Hirsch, 1986). Specific enzymes of Pseudomonasaeruginosa are catalytically active even when cofactornutrients are scarce, and some strains have amanganese-dependent superoxide dismutase whichdoes not require iron and is upregulated at low iron con-centrations (Table 5).

Weeds such as lactic acid bacteria and S. cerevisiaethat lack saprotrophic capabilities can dominate commu-nities in habitats with high nutrient concentrations (Tab-les S1 and 5); they possess high-affinity transportproteins that enable rapid and efficient uptake of substratemolecules to support their vigorous growth phenotypes(see Table 5). Cells of S. cerevisiae are not only highlyefficient at storing carbohydrates (combined trehaloseand glycogen may reach 25% dry weight; Aranda et al.,2004; Guillou et al., 2004), but they can also accumulatehigh concentrations of arginine and polyphosphate andhave adaptations to retain activity under low-nitrogen con-ditions (Table 5). Plant weeds that excel in open habitatshave distinct genetic properties; they are often of hybridorigin and/or polyploid, traits that give rise to increasedgrowth rates and stress tolerance, and have specificgenes that confer their vigorous phenotype (Anderson,1952; Hill, 1977; Schnitzler and Bailey, 2008; Bakkeret al., 2009). There is also evidence that the multiplecopies of genomic material found in vigorous microbesthat enhanced vigour have arisen via hybridization and/orincreased ploidy levels in bacterial weed species, as wellas Pichia and Saccharomyces (Table 5; Cox, 2004). Arecent study by Timberlake and colleagues (2011)reported vigorous growth for the majority of F1 hybridsproduced by crossing 16 wild-type S. cerevisiae strains(although hybridization and/or polyploidy may not alwaysbe advantageous; see Table 5). Many microbial weedspecies are phenotypically variable (like their plant coun-terparts; Table 1; Hill, 1977) and may form part of aspecies complex due to polyploidization and hybridization(e.g. Acinetobacter, Pseudomonas, Mycobacterium, Sac-charomyces sensu stricto; Table S1; Rainieri et al., 1999;Todd et al., 2004; Ballerstedt et al., 2007; Parkinson et al.,2011; Sicard and Legras, 2011); such factors may con-tribute to the vigour and weediness of such species.

High-Mr macromolecules are the primary microbialsubstrates available in many habitats: e.g. hydrocarbons(in bioaerosols, oil-containing environments, and therhizosphere), and polysaccharides (within or derivedfrom plant necromass such as cellulose, lignin and humic



substances; see Table S1). In order to out-compete otherspecies in such habitats, microbes must utilize these mac-romolecular substrates that typically have a low bioavail-ability, require specialist enzymes to degrade, can betoxic, and/or are energy-expensive to catabolize. Faculta-tively saprotrophic microbes such as Aspergillus, Pichia,Rhodotorula and Acinetobacter species are able toaccess and catabolize recalcitrant polysaccharides; someweed species can produce exceptional amounts, or high-affinity versions, of inducible saprotrophic enzymes, suchas xylanases (Table 5). Several saprotrophic enzymesproduced by Aspergillus species (that can dominatephysicochemically diverse habitats; Table S1) can retainactivity over a wide range of environmental stresses(Hong et al., 2001); and Aspergillus, and Rhodotorulaspp. are able to utilize a broad range of nitrogen sub-strates thereby avoiding the need for de novo synthesis(Table 5). Whereas nutritionally complex habitats canselect for metabolic versatility (see below) and therebyfavour the growth of a great number of generalist species,only a minute fraction of such microbes are able to domi-nate what were (initially) phylogenetically diverse micro-bial communities (Table S1).

Antimicrobial strategies and trophic interactions

Grazing, predation and viral infections adversely impactthe growth dynamics of and/or incur massive losses onmicrobial populations and so exert a powerful selectivepressure, and this can be well illustrated by the ecologies ofmany planktonic species in aquatic habitats (Matz et al.,2004; Jüttner et al., 2010; Berdjeb et al., 2011; Thomaset al., 2011; Yang and Kong, 2012). The competitive abilityof some aquatic bacteria and eukaryotes (both marine andfreshwater species) is associated with their ability to resistor tolerate virus infection (see Table 6). Species with ahalophilic growth phenotype, especially those which havehigh growth rates in salt-saturated environments such asS. ruber and H. walsbyi minimize losses to predatorsbecause these salt concentrations are hostile to protozoadue to their low water activity, high ionic strength, and/or(for high-MgCl2 and high-CaCl2 brines) high chaotropicity(Table 6; Hallsworth et al., 2007). Gonyostomum semenhas evolved vertical migration patterns through the watercolumn that are out of phase with those of grazing speciesand thereby minimizes losses (Table 6). Other weeds,including P. aeruginosa and M. aeruginosa, are capable offorming multicellular structures – micrcolonies – that aresufficiently large to reduce losses by many species ofgrazers and predators (Table 6). Species such as M. ae-ruginosa accumulate toxic metabolites, and M. aeruginosaand Aspergillus spp. are known to synthesize secondarymetabolites that repel to grazing plankton and arthropodsrespectively (Table 6).

A number of agricultural (plant) weeds are able to domi-nate their habitats due largely to the production of phyto-toxic inhibitors that can be exuded from leaves, roots andplant necromass and which inhibit the germination and/orgrowth of other plant species (Hill, 1977; Xuan et al., 2006;Alsaadawi and Salih, 2009; Chou, 2010; Meksawat andPornprom, 2010; Inderjit et al., 2011). It is likely that mostmicrobial weed species also secure their competitiveadvantage – in part at least – via the deployment ofantimicrobial substances. Assuming that the exampleslisted in Table S1 are representative of the microbial bio-sphere then the proportion of habitats dominated byeukaryotic species is approximately 40%. If a short gen-eration time was sufficient to facilitate habitat dominationthen prokaryotic species would populate almost all thesehabitats. The fact that species of algae, fungi and yeast arealso able to do so underscores the importance of factorsother than generation time in the biology of habitat domi-nance. Saccharomyces cerevisiae provides an illustrationof how one weed species combines the synthesis of apotent antimicrobial, energy generation, and coordinatedsynthesis of stress protectants in a single process, i.e.aerobic production of the chaotropic alcohol, ethanol (seeabove; Table 6). Ethanol can be produced and secreted atconcentrations > 4 M that cause a reduction of water activ-ity (to 0.896) and exert an exceptionally high chaotropicactivity (see above) sufficient to prevent the growth ormetabolism of any living system (Hallsworth, 1998;Hallsworth and Nomura, 1999; Hallsworth et al., 2007);S. cerevisiae simultaneously produces glycerol (whichcan reduce ethanol stress in yeast and fungi; Hallsworth,1998; Hallsworth et al., 2003b) during ethanol fermenta-tion and is metabolically wired to synthesize high concen-trations of the protectant trehalose at the end of its growthcycle when ethanol concentration is highest (see Table 6).

We believe that the bulk production and secretion ofchaotropic solutes and organic acids (that can reachmolar concentrations) is unique to microbial weed species(Tables 1 and 6). Whereas chaotropic substances canpromote growth and expand the biotic windows ofmicrobes under specific conditions (Hallsworth andMagan, 1994b; 1995; Williams and Hallsworth, 2009;Bhaganna et al., 2010; Chin et al., 2010), in other circum-stances chaotropicity can be highly inhibitory or evenlethal (Hallsworth, 1998; Hallsworth et al., 2003a; 2007;Duda et al., 2004; Bhaganna et al., 2010). For plantweeds it is the early stages of habitat colonization that arekey to their success (Hill, 1977), and is may be that theefficient synthesis of antimicrobials is frequently as impor-tant as much as the type of substance produced(Hallsworth, 1998; Pretorius, 2000; Eshkol et al., 2009;Fialho et al., 2011). Unlike plant weeds, where phyto-toxic inhibitors tend to have the greatest impact onneighbouring plants, microbes can also produce volatile



Tab

le6.

Ant

imic

robi

alac

tiviti

esan

dtr

ophi

cin

tera

ctio

ns:

cellu

lar

char

acte

ristic

sth

atco

ntrib

ute

tow

eed-

like

beha

viou

r.a

Met

abol

ites,

prot

eins

,m

olec

ular

char

acte

ristic

s,an

dot

her

trai

tsF

unct

ion(

s)P

heno

typi

ctr

aits

Not

esan

dre

fere

nces

Avo

idan

ceo

f/re

sist

ance

tovi

ral

infe

ctio

n,

pre

dat

ors

,an

dg

raze

rsM

etab

olite

sth

atre

pelg

raze

rsan

d/or

pred

ator

s,e.

g.al

dehy

des

and

othe

rvo

latil

eor

gani

cco

mpo

unds

inpl

ankt

onan

dfu

ngi

Sec

onda

rym

etab

olite

spr

oduc

edby

Asp

ergi

llus

spp.

repe

l(an

dca

nre

duce

the

fecu

ndity

of)

graz

ing

arth

ropo

dssu

chas

Fol

som

iaca

ndid

a;th

ose

prod

uced

byM

icro

cyst

isae

rugi

nosa

act

asa

repe

llent

topl

ankt

onic

graz

ers

Abi

lity

tore

pelg

raze

rsan

dpr

edat

ors

Asp

ergi

llus

nidu

lans

mut

ants

lack

ing

the

laeA

gene

,a

glob

alre

gula

tor

ofse

cond

ary

met

abol

itesy

nthe

sis,

are

cons

umed

byF.

cand

ida

inpr

efer

ence

toth

ew

ild-t

ype

stra

in(R

ohlfs

etal

.,20

07).

Ald

ehyd

espr

oduc

edby

plan

kton

repe

lcru

stac

ean

graz

ers

(Jüt

tner

,20

05);

b-cy

cloc

itral

from

M.a

erug

inos

aha

sbe

ensh

own

tore

pelD

aphn

iam

agna

(Jüt

tner

etal

.,20

10)

Syn

thes

isof

extr

acel

lula

rpo

lym

eric

subs

tanc

es(e

.g.

M.a

erug

inos

a),

orus

eof

flage

lla(e

.g.

Pse

udom

onas

aeru

gino

sa),

that

faci

litat

em

icro

colo

nyfo

rmat

ion

For

mat

ion

ofm

ultic

ellu

lar

stru

ctur

esth

atar

esu

ffici

ently

larg

eto

min

imiz

egr

azin

gan

dpr

edat

ion

bysi

ngle

-cel

led

prot

ozoa

,zo

opla

nkto

net

c.

Mic

roco

lony

form

atio

nT

hero

leof

poly

mer

icsu

bsta

nces

inco

lony

form

atio

nha

sbe

enes

tabl

ishe

dus

ing

M.a

erug

inos

aas

am

odel

orga

nism

(Yan

gan

dK

ong,

2012

).F

unct

iona

lana

lysi

sof

P.ae

rugi

nosa

mut

ants

that

wer

eun

able

tofo

rmfla

gella

,or

wer

eal

gina

te-d

efici

ent,

dem

onst

rate

dan

inab

ility

tofo

rmm

icro

colo

nies

that

can

conf

erre

sist

ance

togr

azin

g(M

atz

etal

.,20

04)

Bio

chem

ical

adap

tatio

nsto

resi

stvi

rali

nfec

tion

Div

erse

mec

hani

sms

incl

udin

gm

odifi

catio

nof

cell

surf

ace

topr

even

tbi

ndin

g,in

trac

ellu

lar

supp

ress

ion

orvi

ralg

enom

ere

plic

atio

n,an

dde

grad

atio

nof

vira

lDN

Aby

rest

rictio

nen

donu

clea

ses

Res

ista

nce

toor

tole

ranc

eof

vira

lin

fect

ion

The

rear

ea

num

ber

ofm

echa

nism

sby

whi

chdo

min

atin

gsp

ecie

sof

bact

eria

and

euka

ryot

icpl

ankt

on(e

.g.

P.ae

rugi

nosa

,O

stre

ococ

cus

taur

i;B

athy

cocc

usan

dM

icro

mon

assp

p.)

may

acqu

irean

dm

aint

ain

resi

stan

ceto

vira

linf

ectio

n(s

eeT

hom

aset

al.,

2011

;S

elez

ska

etal

.,20

12)

Toxi

cm

etab

olite

s(e

.g.

mic

rocy

stin

inM

.aer

ugin

osa)

Toxi

city

agai

nst

graz

ing

orpr

edat

ory

zoop

lank

ton

Abi

lity

topr

otec

tag

ains

tex

cess

ive

graz

ing

Mic

rocy

stin

synt

hesi

sin

M.a

erug

inos

aca

nbe

indu

ced

byex

posu

reto

zoop

lank

ton;

conc

entr

atio

nsof

the

toxi

nin

cells

expo

sed

toD

.mag

na,

Dap

hnia

pule

xan

dM

oina

mac

roco

paw

ere

upto

fivef

old

thos

efo

und

inco

ntro

lcel

ls(J

ang

etal

.,20

03)

Hal

ophi

licgr

owth

phen

otyp

eC

olon

izat

ion

ofsa

lt-sa

tura

ted

habi

tats

that

are

host

ileto

pred

ator

ypr

otoz

oam

inim

izes

loss

esfr

omgr

azin

gan

dpr

edat

ion

Abi

lity

toin

habi

ten

viro

nmen

tsho

stile

topr

edat

ors

and

graz

ers

Hal

ophi

les

that

dom

inat

ehi

gh-s

alt

habi

tats

(e.g

.D

.sa

lina,

S.r

uber

)m

inim

ize

inte

ract

ions

with

graz

ers

and

pred

ator

sm

ost

ofw

hich

cann

otto

lera

tem

olar

salt

conc

entr

atio

ns(B

arda

vid

etal

.,20

08)

Bio

chem

ical

and

cellu

lar

infr

astr

uctu

reth

atgi

veris

eto

idio

sync

ratic

mig

ratio

npa

ttern

sin

the

wat

erco

lum

n

Ver

tical

mig

ratio

nw

ithin

the

wat

erco

lum

nth

atm

inim

izes

loss

thro

ugh

pred

atio

nan

dgr

azin

g

Avo

idan

ceof

pred

ator

san

dgr

azer

sT

hepr

edom

inan

ceof

Gon

yost

omum

sem

enin

eutr

ophi

cha

bita

tsha

sbe

enas

soci

ated

inpa

rtw

ithm

igra

tion

patte

rns

that

min

imiz

elo

ssth

roug

hgr

azin

g(S

alon

enan

dR

osen

berg

,20

00)

Bu

lkp

rod

uct

ion

of

hig

hly

solu

ble

,m

od

erat

ely

chao

tro

pic

stre

sso

rsb

Eth

anol

prod

uced

via

ahi

gh-K

m

alco

hold

ehyd

roge

nase

(e.g

.A

dh1

inS

acch

arom

yces

cere

visi

ae)

Effi

cien

tco

nver

sion

ofac

etal

dehy

deto

etha

nol;

inco

ntra

st,

low

-Km

Adh

typi

cally

conv

erts

etha

nolt

oac

etal

dehy

deun

der

invi

voco

nditi

ons

(Piš

kur

etal

.,20

06)

Pro

duct

ion

and

secr

etio

nof

etha

nol

(up

tom

olar

conc

entr

atio

ns)

Eth

anol

,se

cret

edin

quan

tity

bysp

ecie

ssu

chas

S.c

erev

isia

ean

dZ

ymom

onas

mob

ilis,

isa

mod

erat

ely

chao

trop

icsu

bsta

nce

that

isne

vert

hele

ssa

pote

ntst

ress

orat

mill

imol

arto

mol

arco

ncen

trat

ions

(Hal

lsw

orth

,19

98;

Bha

gann

aet

al.,

2010

;C

ray

etal

.,20

13)

Enz

ymes

for

acet

one,

isop

ropa

nol

and

buta

nols

ynth

esis

Syn

thes

isof

chao

trop

icsu

bsta

nces

inth

ean

aero

bic

bact

eriu

mC

lost

ridiu

mac

etob

utyl

icum

Bul

kpr

oduc

tion,

and

secr

etio

n,of

mul

tiple

chao

trop

icst

ress

ors

Ace

tone

,is

opro

pano

land

buta

nolt

hat

are

prod

uced

byC

.ac

etob

utyl

icum

(Geo

rge

etal

.,19

83)

are

mor

ech

aotr

opic

etha

nol–

whe

nco

mpa

red

ona

mol

arba

sis

–an

dar

eth

eref

ore

mor

epo

tent

inth

eir

inhi

bito

ryac

tivity

asce

llula

rst

ress

ors

(Bha

gann

aet

al.,

2010

;C

ray

etal

.,20

13;

Bel

leta

l.,20

13)

Pro

duct

ion

ofhi

ghco

ncen

trat

ions

ofur

eaan

dam

mon

iaS

ynth

esis

oflo

w-M

r,ni

trog

enou

sch

aotr

opes

Pro

duct

ion

and

secr

etio

nof

urea

and

amm

onia

atin

hibi

tory

conc

entr

atio

ns

Ure

aan

dam

mon

iaar

epr

oduc

edby

phyl

ogen

etic

ally

dive

rse

bact

eria

such

asP

seud

omon

asst

utze

rian

dC

lost

ridiu

mam

inop

hilu

mre

spec

tivel

y(T

herk

ildse

net

al.,

1997

;W

atan

abe

etal

.,19

98;A

nder

son

etal

.,20

10)

Rel

ease

of

VO

Cs

aslo

w-s

olu

bili

tyan

tim

icro

bia

lst

ress

ors

Hig

hly

vola

tile

met

abol

ites

that

act

ashy

drop

hobi

cst

ress

ors

(log

P>

1.95

)c

Inhi

bitio

nof

mic

robi

alm

etab

olis

m;

typi

cally

via

hydr

ocar

bon-

indu

ced

wat

erst

ress

(Bha

gann

aet

al.,

2010

)

Pro

duct

ion

and

rele

ase

ofvo

latil

ean

timic

robi

als

Exa

mpl

esar

e:is

oam

ylac

etat

e(p

rodu

ced

byP

ichi

aan

omal

a;P

asso

thet

al.,

2006

),et

hyl

octa

noat

e(S

.ce

revi

siae

;F

ialh

oet

al.,

2011

),b-

cycl

ocitr

al(M

.aer

ugin

osa

and

Dun

alie

llasa

lina;

Her

rero

etal

.,20

06;

Oza

kiet

al.,

2008

),pe

ntan

e(D

.sal

ina;

Muñ

ozet

al.,

2004

);an

ddi

vers

esu

bsta

nces

from

Asp

ergi

llus

(see

abov

e),

R.m

ucila

gino

sa(B

uzzi

niet

al.,

2005

),P.

putid

aan

dot

her

Pse

udom

onas

spec

ies

(Mor

ales

etal

.,20

05)

Hig

hly

vola

tile,

stro

ngly

chao

trop

icm

etab

olite

s(lo

gP

typi

cally

inth

era

nge

1–1.

9)c

Inhi

bitio

nof

mic

robi

alm

etab

olis

mvi

ach

aotr

ope-

indu

ced

wat

erst

ress

(Hal

lsw

orth

,19

98;

Hal

lsw

orth

etal

.,20

03a;

Bha

gann

aet

al.,

2010

)

Pro

duct

ion

and

rele

ase

ofvo

latil

ean

timic

robi

als

Exa

mpl

esar

e:et

hyla

ceta

te(p

rodu

ced

byP

ichi

aan

omal

a;W

alke

r,20

11),

dich

loro

met

hane

(Dun

alia

llasp

p.;

Col

omb

etal

.,20

08)

and

2-ph

enyl

etha

nol(

Myc

obac

teriu

mbo

vis,

Myc

obac

teriu

msm

egm

atis

and

S.

cere

visi

ae;

Esh

kole

tal.,

2009

;M

cNer

ney

etal

.,20

12);

and

ara

nge

ofch

aotr

opic

stre

ssor

sby

R.m

ucila

gino

sa(B

uzzi

niet

al.,

2005

),P.

putid

aan

dot

her

Pse

udom

onas

spec

ies

(Mor

ales

etal

.,20

05)



Vol

atile

cata

bolit

espr

oduc

edfr

omth

ede

grad

atio

nof

mac

rom

olec

ular

subs

trat

es

Inhi

bitio

nof

mic

robi

alm

etab

olis

mty

pica

llyvi

ach

aotr

ope-

indu

ced

orhy

droc

arbo

n-in

duce

dw

ater

stre

ss(H

alls

wor

thet

al.,

2003

a;B

haga

nna

etal

.,20

10)

Pro

duct

ion

and

rele

ase

ofvo

latil

ean

timic

robi

alsg

Ant

imic

robi

alst

ress

ors

can

bere

leas

eddu

ring

the

sapr

otro

phic

degr

adat

ion

oflig

nin,

cata

bolis

mof

hydr

ocar

bons

etc.

(e.g

.ca

tech

ol,

vani

llin

and

biph

enyl

inP.

putid

a;Z

urof

fan

dC

urtis

,20

12)

Aci

difi

cati

on

of

the

extr

acel

lula

ren

viro

nm

ent

Sec

retio

nof

orga

nic

acid

sA

cidi

ficat

ion

ofth

eex

trac

ellu

lar

mili

euA

bilit

yto

acid

ifyth

eha

bita

tA

cine

toba

cter

rhiz

osph

aera

ean

dS

.cer

evis

iae

secr

ete

ara

nge

ofsu

bsta

nces

that

can

acid

ifyth

een

viro

nmen

t(K

otyk

etal

.,19

99;

Gul

atie

tal.,

2010

);A

sper

gillu

ssp

p.pr

oduc

eshi

ghle

vels

ofci

tric

acid

(up

to20

0g

l-1in

5–7

days

;W

ard

etal

.,20

06)

Hig

h-ac

tivity

L-la

ctat

ede

hydr

ogen

ase

(e.g

.ld

hLin

Lact

obac

illus

plan

taru

m)

Intr

acel

lula

rco

nver

sion

ofpy

ruva

teto

lact

ate

Pro

duct

ion

and

secr

etio

nof

lact

icac

idT

hesp

ecifi

cac

tivity

ofId

hLfr

oma

lact

icac

idpr

oduc

edby

L.pl

anta

rum

was

foun

dto

be24

60U

mg-1

;co

mpa

red

with

250

Um

g-1fo

rE

sche

richi

aco

li(G

arvi

e,19

80).

Hab

itat

acid

ifica

tion

byla

ctic

acid

inhi

bits

the

grow

thof

man

ym

icro

bial

com

petit

ors

(Tab

leS

1;G

uillo

tet

al.,

2003

).La

ctob

acill

usef

ficie

ntly

acid

ifies

itsen

viro

nmen

tev

enat

low

suga

rco

ncen

trat

ions

(Klin

keet

al.,

2009

)E

nzym

esfo

rac

etic

and

buty

ricac

idsy

nthe

sis

(e.g

.ph

osph

otra

nsac

etyl

ase

and

acet

ate

kina

se,

and

phos

phat

ebu

tyry

ltran

sfer

ase

and

buty

rate

kina

sere

spec

tivel

y)

Con

vers

ion

ofac

etyl

-CoA

toac

etat

e;an

dbu

tyry

l-CoA

tobu

tyra

teP

rodu

ctio

n/se

cret

ion

ofac

etic

acid

and

buty

ricac

idC

lost

ridiu

msp

p.pr

oduc

eac

etic

,bu

tyric

and

lact

icac

ids;

ferm

enta

tions

carr

ied

out

inm

edia

with

anin

itial

pHof

~6.

5re

sulte

din

afin

alpH

of4–

4.5

(Wie

senb

orn

etal

.,19

89;

Boy

nton

etal

.,19

96;

Liu

etal

.,20

11)

Pro

du

ctio

no

fb

iosu

rfac

tan

ts,

enzy

mes

,an

d/o

rto

xin

sw

ith

anti

mic

rob

ial

acti

viti

esB

iosu

rfac

tant

s(e

.g.

rham

nolip

ids

inP

seud

omon

assp

p.;

glyc

olip

opro

tein

sin

Asp

ergi

llus

spp.

)

Sol

ubili

zatio

nof

hydr

opho

bic

subs

trat

es;

inhi

bito

ryto

the

grow

thof

man

ym

icro

bial

com

petit

ors

Pro

duct

ion

ofin

hibi

tory

bios

urfa

ctan

tsLi

pope

ptid

esfr

omP

seud

omon

assp

.D

F41

wer

esh

own

toin

hibi

tS

cler

otin

iasc

lero

tioru

m(B

erry

etal

.,20

10);

purifi

edbi

osur

fact

ants

from

Pse

udom

onas

fluor

esce

nsin

hibi

tgr

owth

ofB

otry

tisci

nere

aan

dR

hizo

cton

iaso

lani

atlo

wco

ncen

trat

ions

(25

mgm

l-1)

and

can

lyse

zoos

pore

sof

Phy

toph

thor

aca

psic

i(K

ruijt

etal

.,20

09).

Stu

dies

ofP.

aeru

gino

sarh

amno

lipid

sugg

ests

ake

yro

lein

com

petit

ive

abili

tyag

ains

tot

her

bact

eria

(Wec

keet

al.,

2011

).A

cine

toba

cter

spp.

prod

uces

apo

tent

bios

urfa

ctan

t(p

hosp

hatid

ylet

hano

lam

ine;

Des

aian

dB

anat

,19

97)

whi

chm

ayac

tas

anan

timic

robi

al.

Bio

surf

acta

nts

from

Asp

ergi

llus

ustu

sar

ein

hibi

tory

toph

ylog

enet

ical

lydi

vers

em

icro

bes

(Kira

net

al.,

2009

)P

anom

ycoc

in(a

nex

o-b-

1,3-

gluc

anas

e)H

ydro

lysi

sof

gluc

ans

such

asla

min

arin

Ant

imic

robi

alan

dcy

toci

dala

ctiv

ityvi

ade

grad

atio

nof

cell

wal

lco

mpo

nent

s

Pan

omyc

ocin

ispr

oduc

edby

P.an

omal

aan

dis

inhi

bito

ryor

leth

alto

man

ysp

ecie

sof

yeas

tsan

dfu

ngis

uch

asB

.cin

erea

(Izg

üet

al.,

2005

)

Och

rato

xin

and

othe

rm

ycot

oxin

s(e

.g.

inA

sper

gillu

ssp

p.)

Inhi

bitio

nof

othe

rm

icro

bial

spec

ies/

stra

ins

Sec

retio

nof

antim

icro

bial

sM

ycot

oxin

sca

nin

hibi

tph

ylog

enet

ical

lydi

vers

em

icro

bes

(incl

udin

gfu

ngal

and

bact

eria

lsp

ecie

s)an

dth

ereb

yen

hanc

eco

mpe

titiv

eab

ility

(Bou

tibon

nes

etal

.,19

84;

Mag

anet

al.,

2003

)A

ntifu

ngal

pept

ide

(Ana

fp;

inA

sper

gillu

sni

ger)

Mod

e-of

-act

ion

not

yet

reso

lved

Sec

retio

nof

anan

tifun

galp

eptid

eA

nafp

inhi

bits

grow

thof

yeas

tsan

dfu

ngii

nclu

ding

som

eA

sper

gillu

san

dF

usar

ium

spp.

,C

andi

daal

bica

ns,

S.c

erev

isia

ean

dTr

icho

spor

onbe

igel

ii(L

eeet

al.,

1999

)M

ycoc

ins

(e.g

.sa

lt-m

edia

ted

kille

rto

xin)

Inhi

bito

ryto

man

yfu

ngi,

yeas

tsan

dot

her

mic

robe

sP

rodu

ctio

nof

antib

iotic

pept

ides

Ara

nge

ofki

ller

toxi

nspr

oduc

edby

Pic

hia

farin

ose,

Rho

doto

rula

spp.

and

S.c

erev

isia

eth

atar

ein

hibi

tory

toph

ylog

enet

ical

lydi

vers

eta

xa(G

olub

evan

dC

hurk

ina,

1993

;;G

olub

evet

al.,

1996

;S

uzuk

ieta

l.,20

01;

Trin

dade

etal

.,20

02;A

lber

garia

etal

.,20

10)

Bac

terio

cins

e.g.

plan

tarc

ins

(pln

gene

fam

ily),

lact

acin

-B(L

a179

1–La

1803

),pl

ant

lect

in-li

keba

cter

ioci

n(L

lpA

)

Mod

ifica

tion

ofm

embr

ane

stru

ctur

eca

usin

gle

akag

ean

ddi

ssip

atio

nof

prot

on-m

otiv

efo

rce

(And

erss

enet

al.,

1998

;P

arre

tet

al.,

2003

;Alte

rman

net

al.,

2005

)

Pro

duct

ion

ofan

tibac

teria

lpep

tides

For

exam

ple

L.pl

anta

rum

,La

ctob

acill

usac

idop

hilu

san

dP

seud

omon

assp

p.

Pyo

lute

orin

(inP.

putid

a)In

hibi

tory

togr

owth

ofoo

myc

etes

and

fung

i;m

ode-

of-a

ctio

nno

tye

tre

solv

edA

ntifu

ngal

activ

ityP

yolu

teor

in-p

rodu

cing

P.pu

tida

stra

ins

have

pote

ntia

las

bioc

ontr

olag

ents

ofpa

thog

ens

such

asG

lom

erel

latu

cum

anen

sis

(sug

arca

nere

dro

t;N

owak

-Tho

mps

onet

al.,

1999

;H

assa

net

al.,

2011

)P

hena

zine

and

phen

azin

e-de

rived

antim

icro

bial

sP

roba

ble

antim

icro

bial

activ

ityA

ntim

icro

bial

activ

ityP

rodu

ced

bysp

ecie

ssu

chas

M.a

erug

inos

aan

dP.

aeru

gino

sa(M

avro

diet

al.,

2006

;Li

fshi

tsan

dC

arm

eli,

2012

)M

echa

nism

sto

indu

cece

llly

sis

Elim

inat

ion

ofpo

tent

ialc

ompe

titor

sA

lgic

idal

activ

ityG

onyo

stom

umse

men

isab

leto

lyse

mic

robi

alce

lls(e

.g.

Rho

dom

onas

lacu

stris

)on

cont

act;

mec

hani

smno

tye

tre

solv

ed(R

enge

fors

etal

.,20

08)

Res

ista

nce

toan

tim

icro

bia

lst

ress

ors

and

toxi

ns

Coo

rdin

ated

prod

uctio

nof

com

patib

leso

lute

san

det

hano

lP

rote

ctio

nag

ains

tet

hano

lstr

ess

Res

ista

nce

toet

hano

lT

hesy

nthe

sis

ofgl

ycer

ol(k

now

nto

affo

rdso

me

prot

ectio

nag

ains

tet

hano

lstr

ess;

Hal

lsw

orth

,19

98;

Hal

lsw

orth

etal

.,20

03b)

and

etha

nolp

rodu

ctio

nar

eco

uple

din

S.

cere

visi

ae;

accu

mul

atio

nof

treh

alos

e(a

nef

fect

ive

prot

ecta

ntag

ains

tet

hano

l;M

ansu

reet

al.,

1994

)co

inci

des

with

the

grow

thph

ase

whe

net

hano

lcon

cent

ratio

nsar

ehi

ghes

t



Tab

le6.

cont

.

Met

abol

ites,

prot

eins

,m

olec

ular

char

acte

ristic

s,an

dot

her

trai

tsF

unct

ion(

s)P

heno

typi

ctr

aits

Not

esan

dre

fere

nces

Com

patib

le-s

olut

eac

cum

ulat

ion

inre

spon

seto

solv

ent

and

hydr

opho

bic

stre

ssor

s(s

eeab

ove)

Pro

tect

ion

ofm

acro

mol

ecul

arsy

stem

sch

alle

nged

bych

aotr

opic

and

hydr

opho

bic

stre

ssor

s(s

eest

udie

sof

A.n

idul

ans,

S.c

erev

isia

ean

dP.

putid

a:M

ansu

reet

al.,

1994

;H

alls

wor

thet

al.,

2003

b;P

ark

etal

.,20

07;

Bha

gann

aet

al.,

2010

;B

ell

etal

.,20

13)

Abi

lity

tom

aint

ain

func

tiona

lity

ofm

acro

mol

ecul

arsy

stem

sK

osm

otro

pic

com

patib

le-s

olut

esan

dot

her

kosm

otro

pic

subs

tanc

esca

nre

duce

stre

ssin

duce

dby

chao

trop

icso

lute

ssu

chas

MgC

l 2,

glyc

erol

dan

det

hano

l(H

alls

wor

th,

1998

;H

alls

wor

thet

al.,

2007

;W

illia

ms

and

Hal

lsw

orth

,20

09).

Tryp

toph

anan

dtr

ehal

ose

are

upre

gula

ted

ince

llsof

both

euka

ryot

ican

dba

cter

ials

peci

esin

resp

onse

toet

hano

l(P

arro

uet

al.,

1997

;P

urvi

set

al.,

2005

;H

irasa

wa

etal

.,20

07;

Hor

inou

chie

tal.,

2010

).S

.cer

evis

iae

coul

dto

lera

te28

%v/

vet

hano

lwhe

npr

otec

ted

byth

eko

smot

ropi

cco

mpa

tible

-sol

ute

prol

ine

(Tho

mas

etal

.,19

93;

Hal

lsw

orth

,19

98)

Upr

egul

atio

nof

prot

ein-

stab

iliza

tion

prot

eins

(see

Tabl

e3)

Pro

tect

ion

ofm

acro

mol

ecul

arsy

stem

sfr

ompe

rtur

batio

nsin

duce

dby

antim

icro

bial

stre

ssor

s

Mai

nten

ance

ofpr

otei

nst

ruct

ure

and

func

tion

durin

gst

ress

or-in

duce

dch

alle

nges

Sac

char

omyc

esce

revi

siae

upre

gula

tes

synt

hesi

sof

upto

10he

at-s

hock

prot

eins

unde

ret

hano

lstr

ess

(Ma

and

Liu,

2010

).P

seud

omon

aspu

tida

synt

hesi

zes

dive

rse

prot

ein-

stab

iliza

tion

prot

eins

inre

spon

seto

chao

trop

ican

dhy

drop

hobi

cst

ress

ors

(see

abov

e;H

alls

wor

thet

al.,

2003

a;B

haga

nna

etal

.,20

10)

Mem

bran

e-st

abili

zatio

npr

otei

ns;

solv

ent

pum

ps(s

eeTa

ble

3)M

ultid

rug

efflu

xpu

mps

(e.g

.A

crA

B-T

olC

inE

.col

i;P

dr5p

inS

.cer

evis

iae;

AB

Ctr

ansp

orte

rpr

otei

nsin

Asp

ergi

llus

spp.

)

Exp

ulsi

onof

chem

ical

lydi

vers

est

ress

ors

and

toxi

nsTo

lera

nce

toa

wid

ear

ray

ofst

ress

ors

and

toxi

nsIn

clud

ing

chao

trop

icso

lute

s(e

.g.

phen

ol,

benz

ylal

coho

l),hy

drop

hobi

cst

ress

ors

(e.g

.n-

hexa

ne,

p-xy

lene

)an

dan

tibio

tics

(e.g

.ch

lora

mpe

nico

l,te

trac

yclin

e,no

vobi

ocin

)by

Acr

AB

-Tol

C;

fluor

esce

ntdy

es(e

.g.

daun

orub

icin

,rh

odam

ine)

,dr

ugs

(e.g

.ta

mox

ifen)

;an

dio

noph

oric

pept

ides

(e.g

.ni

geric

in)

byP

dr5p

(Kol

aczk

owsk

ieta

l.,19

96);

and

antif

unga

ls(c

ilofu

ngin

and

echi

noca

ndin

B)

byth

eA

fuM

DR

1ge

nepr

oduc

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organic compounds (VOCs) that inhibit the growth of bothproximal and distal cells via their dispersion in bothaqueous and gaseous milieu (Table 6).

Volatile organic compounds – including aldehydes,furones, terpenes and many alcohols – can be powerfulinhibitors of microbial metabolism and growth (Table 6;Jorge and Livingston, 1999; Passoth et al., 2006; Minerdiet al., 2009; Fialho et al., 2011; Corcuff et al., 2011).Despite their volatility they are to some degree also water-soluble, and are sufficiently inhibitory to prevent metabolicactivity and growth, even in aqueous solution at subsatu-rated solute-concentrations (Bhaganna et al., 2010).VOCs with a log Poctanol-water < 1.95 typically partition intothe aqueous phase of cellular macromolecules and canact as potent chaotropic stressors (Table 6; Hallsworthet al., 2003a; Bhaganna et al., 2010; Cray et al., 2013).Those stressors with a log P of > 1.95 preferentially par-tition into the hydrophobic domains of membranesand other macromolecular systems, and thereby act ashydrophobic stressors that induce a distinct type ofchaotropicity-mediated water stress (Bhaganna et al.,2010). We believe that the primary ecophysiological valueof VOCs for microbial cells pertains to competition,species succession and (for weed species) habitat domi-nance. Saccharomyces cerevisiae synthesizes bothhydrophobic and chaotropic volatiles that have antimicro-bial activities, including ethyl octanoate and isoamylacetate, and ethyl acetate and 2-phenylethanol (respec-tively, see Table 6; Fialho et al., 2011). Ethanol and2-phenylethanol are synergistic in their antimicrobial activ-ity (Ingram and Buttke, 1984; Seward et al., 1996), andthis is consistent with their common chaotropicity-mediated mode-of-action. The more potent chaotrope ofthe two (when compared on a molar basis) is2-phenylethanol which prevents growth of microbes in therange 10–40 mM (Berrah and Konetzka, 1962; Eshkolet al., 2009), values consistent with a chaotropic mode-of-action for a stressor with a log P of 1.36 (see Bhagannaet al., 2010). Saccharomyces cerevisiae (like P. anomala,Acinetobacter and lactic acid bacteria) also inhibits thegrowth of competing species by acidifying the environ-ment which it achieves via the production of a number oforganic acids (Table 6; Kotyk et al., 1999; Lowe andArendt, 2004; Gulati et al., 2010); it also secretes peptideswith fungicidal and fungistatic activities (Albergaria et al.,2010); and some strains contain inheritable virus-like par-ticles containing genes that code for proteins inhibitory toother strains of the same species (Pretorius, 2000). Notonly does S. cerevisiae employ multiple types of antimi-crobial substance that act in concert, it is also has acorrespondingly wide range of stressor-protection meas-ures that minimize metabolic inhibition by antimicrobialstressors (those synthesized by either S. cerevisiae orother species), including efflux pumps (Pretorius, 2000),

and highly effective compatible-solute strategies (seeabove), protein-stabilization proteins and adaptations toacid stress (Table 6) and is therefore highly toleranttowards chaotropic and hydrophobic stressors (Fig. 2;Tables 4 and 6). Saccharomyces cerevisiae acid toler-ance (as well as that of lactic acid bacteria) is conferred byan array of mechanisms (Table 3) that collectively contrib-ute to the weed phenotype by removing the hydrogen ionsand/or by promoting the refolding of partially denaturedbiomacromolecules.

Pichia anomala utilizes an array of antimicrobials thathave synergistic effects as inhibitors and collectively targeta wide array of taxa (including fungi, other yeasts, bacteriaand viruses; Walker, 2011): chaotropic stressors such asethanol and ethyl acetate; hydrophobic stressors such asisoamyl acetate; biosurfactants (see below); organicacids; an exo-b-1,3-glucanase known to degrade glucansin fungal cell walls; and diverse toxins that have specificmodes-of-action (see Table 6; Passoth et al., 2006;Walker et al., 2011). A semi-quantitative analysis of theantifungal activities of P. anomala suggests that inhibitionresults primarily from a combination of (in order of impor-tance): killer toxins, hydrolytic enzymes and volatile sub-stances (Table 6), as well as more minor factors such asnutrient competition and substrate acidification (Walker,2011). Rhodotorula mucilaginosa produces an array ofvolatile chaotropic and hydrophobic stressors as well askiller toxins (Table 6). Many fungi also produce mycotox-ins; for example Aspergillus ochraceus growing on maizegrain can produce ochratoxins at up to 1.4 mg g-1 (Maganet al., 2003). Indeed a number of Aspergillus species arenotorious for the potent activity of their ochratoxins againstother fungal strains and as well as bacteria (Table 6).

Like S. cerevisiae, some other microbial species areable to produce moderately chaotropic antimicrobials inbulk quantities: Clostridium acetobutylicum produces highconcentrations of butanol, ethanol and acetone in anaero-bic habitats, and Zymomonas mobilis produces high con-centrations of ethanol (Tables S1 and 6). Butanol is aparticularly potent chaotrope that is highly inhibitory atmillimolar concentrations (Bhaganna et al., 2010; Ezejiet al., 2010; Cray et al., 2013). We suspect that Clostrid-ium spp. that can dominate chaotropic environments suchas ammonia-rich animal slurries (Table S1) have an unu-sually high resistance to the net chaotropicity of theammonia, ethanol, butanol, acetone and other chaotropicsubstances in their habitat (a hypothesis that has not yetbeen investigated to our knowledge; Williams andHallsworth, 2009; Cray et al., 2013). The chaotropicityof urea and ammonia is greater than that of ethanolwhen compared at equivalent molar concentrations(Hallsworth et al., 2003a; Williams and Hallsworth, 2009)and there is evidence that some bacteria that secretethese compounds, including Clostridium aminophilum and



Pseudomonas stutzeri, benefit from chaotropicity-inducedinhibition of their competitors (Table 6). There is no abso-lute resistance to the inhibitory/lethal activities of chao-tropic and hydrophobic stressors (Sikkema et al., 1995;Hallsworth, 1998; Hallsworth et al., 2003a; 2003b; 2007;Duda et al., 2004; Bhaganna et al., 2010; Bell et al., 2013)so the production of such antimicrobials coupled withreasonably effective self-protection mechanisms (seeTables S1 and 6) can sometimes be the ultimate means toachieve community dominance (see also Table S1).

Pseudomonas putida can generate and/or secretediverse antimicrobial substances including catabolitesproduced from degradation of macromolecular substrates,VOCs and biosurfactants (Table 6). Biosurfactants thatsolubilize hydrocarbons and other hydrophobic substratescan also be highly inhibitory to other microbial species.Studies of Pseudomonas rhamnolipids suggest a key rolein competitive ability (Wecke et al., 2011); surfactants notonly disorder plasma membranes and solubilize lipids, butcan be chaotropic even for macromolecules that lackhydrophobic domains (Table 2; Cray et al., 2013). Themembrane-permeabilizing activities of rhamnolipids areparticularly detrimental to Gram-positive bacteria, and arelethal to Phytophthora zoospores (Kruijt et al., 2009,Wecke et al., 2011). Bacteriocins produced by pseu-domonads, like those of lactic acid bacteria, modify cellu-lar membranes increasing permeability, causing leakage,disrupting transport processes and causing a dissipationof proton-motive force (Table 6). Catabolites such asphenol, catechol, vanillin, biphenyl, and sodium benzoatethat are produced from the degradation of high-Mr hydro-carbons have inhibitory activity as chaotropic and hydro-phobic stressors (Table 6; Hallsworth et al., 2003a;Bhaganna et al., 2010). Pseudomonas putida and otherpseudomonads produce a wide variety of VOCs that col-lectively impact microbial competitors (Table 6). As out-lined above, P. putida has multiple layers of defenceagainst the potential stressful impact of solvent, chao-tropic, and hydrophobic stressors via a versatile compat-ible solute metabolism (e.g. trehalose; Park et al., 2007;Bhaganna et al., 2010), protein-stabilization proteins, andproduction of extracellular polymeric substances etc.(Tables 3 and 6). In addition, and arguably the most impor-tant feature for stressor tolerance, P. putida cells areequipped with efflux pumps (for example the plasmid-encoded TtGHI) that are highly effective at expulsion ofhydrocarbons such as toluene as well as many otherstressors and toxins (Ramos et al., 2002; Fillet et al.,2012).

Whereas the aquatic habitats of planktonic speciessuch as D. salina, G. semen and M. aeruginosa mayserve to dilute secreted antimicrobials, there is evidencethat VOCs produced by D. salina, M. aeruginosa, andother aquatic species (including compounds such as

b-cyclocitral and dichloromethane) are inhibitory to com-peting species (Table 6). Gonyostomum semen is able tolyse the cells of competing algal species on contactalthough the mechanism by which it does so has yet to beresolved (Table 6); and M. aeruginosa synthesizes adiverse range of volatile antimicrobials including phena-zines and phenazine derivatives (Table 6; Lifshits andCarmeli, 2012). Lactic acid bacteria, in addition to bacte-riocins, produce significant quantities of organic acids andsecrete a vast array of inhibitory VOCs (Table 6). Theanalysis of volatiles produced, primarily by L. rhamnosus,during the production of a ewe’s-milk cheese (Table S1)gives an insight into the complexity of the microbial ware-fare that takes place in open habitats: 57 compoundswere detected including terpenes, alcohols, ketones andesters (Randazzo et al., 2010) Although it is plausiblethat some of these substances exert specific toxic effects,all of them have the properties of either chao- or hydro-phobic stressors in microbial cells (Table 6; Bhagannaet al., 2010), and their roles in habitat dominance hasrarely received attention.

Microbial weed ecology

Open habitats

The concept of an open habitat is a fundamental, well-established principle in the fields of plant and animalecology. For microorganisms, open habitats can bedefined according to the diversity, interactions and com-munity succession of their inhabitants in contrast to othertypes of microbial habitat that are defined by physico-chemical characteristics, substrate type or nutrient con-centration (Table 7). Hydrocarbons are the primarycarbon substrate in approximately one-third of the openhabitats listed in Table S1, and are generally derived fromdense, non-aqueous phase liquids (e.g. oil) or plantmetabolites secreted into the rhizosphere, phyllosphereor atmosphere (bioaerosols). A distinguishing feature ofhydrocarbon-based systems is that they can remain per-petually open because, as dissolved hydrocarbons areassimilated, the substrate reservoir may be continuallyreplenished by molecules from the oil entering theaqueous phase or (for the rhizosphere and phyllosphere)because the plant continues to produce and secretehydrocarbons and other organics (Nunes et al., 2005;Kazda and Falkinham III, 2009; McCammick et al., 2009;Hunter et al., 2010; Kachalkin and Yurkov, 2012). Thesehabitats are commonly dominated by species suchas Acinetobacter johnsonii, Alkanivorax borkumensis,Pantoea ananatis and P. putida. Whereas these organ-isms – all members of the gammaproteobacteria – mayshare many molecular and ecophysiological characteris-tics (see Tables S1 and 3–6) in most cases it is P. putidathat emerges as the most prevalent species (Table S1).



Table 7. Properties of open (microbial) habitats.

Typical characteristic(s)

Value as adescriptor foran open habitata

Notes and examples

For open habitats For habitats that are not open

Microbial ecologyOpen to population by a

multitude of microbialspecies

Primary Potentially habitable by an indefinitenumber of species which may befrom diverse Kingdoms of life (e.g.solar salterns see Table S1)

The fracture water of aSouth-African goldmine (2.8 kmdeep) was found to contain asingle-species ecosystem(Chivian et al., 2008)

Promote intense competitionbetween microbialspecies

Primary Conditions favour strong growth ofmany species and may select forability to produce antimicrobialsubstances (see below)

A climax community, single-specieshabitat, and symbioticpartnership are characterized bylow levels of inter-speciescompetition

Can facilitate dominance ofthe developing communityby one or more species(though this may notalways take place)

Primary Diverse types of substrate/environmentcan accommodate communityprogression towards dominance byone or more microbial species (seeTable S1)

The antithesis of an open habitat isone that is occupied by a climaxcommunity that is no longercapable of further evolution (e.g.Paul et al., 2006)

Transient andself-terminating; unlessmaintained in an ‘open’condition

Primary Frequently leading to the developmentof a closed community dominated bya single species (see Fig. 1;Table S1); unless ‘re-opened’ due tograzing for example, or replenished(e.g. by fresh inputs of nutrients)

Closed habitats typically lackconditions that facilitate biomassformation and speciessuccession

Resident microbesStrong selection for

microbes able to out-growcompetitors

Primary For example, habitats rich in nutrientsmay favour species of bacterialcopiotroph which may merge asdominating species if they possessother weed traits

A habitat with limited availableresources would not would notsupport growth (the latter isassociated with competition/species succession)

Open to manipulation byspecies able to modifyenvironmental conditionsand/or secreteantimicrobials

Primary Dynamic biomass formation makesopen habitats available for/vulnerable to manipulation byspecies that can introducegrowth-limiting substances (Table 6;Cordero et al., 2012)

In closed habitats the community isalready restricted in terms ofspace, nutrients and/orphysicochemical constraints etc.

Select for microbes that lackspecific requirements(such as rare traceelements, or a specifichost)

Secondary Microbes such as S. cerevisiae andLactobacillus spp. typically growwithout idiosyncratic requirements(such as a requirement forinteractions with other species)

Specialist microbes are found inniche habitats, such as thosethat form lichens (Hoffland et al.,2004)

Chemistry and properties of the cellular environmentNot excessively stressful for

resistant microbes interms of water activity,chaotropicity, pH,temperature etc.b

Primary Open (microbial) habitats are, bydefinition, open to population by alarge number and high diversity ofmicrobial species so are typically notphysically or chemically extremec

Extreme habitats that are occupiedby a small number of obligateextremophiles rarely support thehigh growth rates or promote theintense competition that typifyopen habitatsc

Have the potential tosupport a substantialmicrobial biomass and sodo not constrainecosystem development

Primary Open habitats have sufficient spaceand resources to facilitate theecosystem development (Table S1;Fig. 1)

Non-open habitats can beconstrained by nutritional and/orphysicochemical parameters(Chivian et al., 2008)

Not contaminated withinhibitory substancessuch as heavy metals orother potent toxins

Secondary Some polluted, hydrocarbon-richenvironments may also support thedevelopment of microbialcommunities

High levels of toxic substances willprevent high growth rates andminimize diversity

a. Those designated as descriptors of primary importance are considered essential to the definition of an open (microbial) habitat.b. Not so extreme that there is limited diversity or possibility for biomass formation: i.e. typically > 0.75 water activity (see Pitt, 1975; Williams andHallsworth, 2009), < 20–25 kJ kg-1 mole-1 chaotropic activity (Hallsworth et al., 2007), < pH 11 or > -15°C.c. Whereas NaCl-saturated habitats are generally considered extreme, their water activity is 3 0.75 – well above that which ultimately limitsmicrobial life (i.e. 0.61–0.71: Pitt and Christian, 1968; Brown, 1990; Grant, 2004; Williams and Hallsworth, 2009; Leong et al., 2011) – andtypically supports a remarkably high microbial diversity and biomass (Antón et al., 2002; Daffonchio et al., 2006; Baati et al., 2008; Bardavidet al., 2008; Khemakhem et al., 2010).



This is a product of its metabolic versatility, exceptionaltolerance to hydrocarbons and other solutes, and antimi-crobial activities (Tables 3, 5 and 6). Other weed species,however, have greater acid tolerance than the gammapro-teobacteria: in the acidic surface film of the sphagnum-moss grey layer it is Mycobacterium (includingMycobacterium terrae, M. smegmatis and Mycobacteriumsphagni) that emerges as a dominant genus; and in thegreen layer at lower pH (2–2.5), R. mucilaginosa has thecompetitive advantage (Table S1). Phyllosphere, rhizo-sphere and other habitats can also remain continuouslyopen if they are replenished with organic substances fromions released from soil particles, extracellular polymericsubstances and compatible solutes from microbial cells,root diffusates, animal wastes, diverse sources of necro-mass, etc.

Habitats which facilitate weed emergence are typicallynot so extreme that there is a negligible microbial diversityor little capacity for community development/biomass for-mation; i.e. > 0.75 water activity, < 20–25 kJ kg-1 mole-1

chaotropic activity, < pH 11 or > -15°C (Table 7). Openhabitats have available nutrients, electron acceptors etcand C : N ratios that favour microbial growth, and do notcontain high levels of inhibitory substances such as heavymetals or toxic pollutants. They will therefore promoteintense competition between species assuming that adiversity of microbial species is present (Tables S1 and 7).Whereas high-sugar habitats with a water activity below0.9 are too stressful for the vast majority of microbes,including S. cerevisiae, there is still a considerable diver-sity of xerotolerant and xerophilic species that are highlyactive between water activities of 0.84 and 0.9 (Pitt, 1975;Brown, 1990). Similarly, crystallizer ponds or solar salt-erns are known as extreme environments and only asmall fraction of microbial species can survive and grow atsaturated NaCl. Nevertheless, it is the limited solubility ofNaCl (and not the limitations of salt-adapted macromo-lecular and cellular systems) that determines the limit formicrobial growth in high-NaCl habitats: a number of obli-gate halophiles grow optimally at 35% w/v NaCl (0.755water activity) and different types of NaCl-saturated envi-ronment are biodiverse, highly competitive, biomass-richmicrobial habitats (Antón et al., 2002; Daffonchio et al.,2006; Baati et al., 2008; Bardavid et al., 2008; Khema-khem et al., 2010). Salterns (and also algal mats) mayunder some conditions function as continually open habi-tats if nutrients are not limiting; D. salina for example canrelease sufficient glycerol into the system to satisfy thecarbohydrate requirement of the wider community(Borowitzka, 1981; Bardavid et al., 2008).

Open habitats favour microbes with shorter generation-times and relatively vigorous growth-phenotypes and inthis way may drive the evolution of faster-growing andmore stress-tolerant species (as well as those with effec-

tive antimicrobial strategies; Tables 4, 6 and 7). That theecology and evolution of plant weeds are intimately andinextricably linked with open habitats has been estab-lished for some time (Anderson, 1952); in contrast there islittle information about open habitats of microorganisms(see Table 1; Hallsworth, 1998). Open habitats can bespontaneously created (e.g. due to removal of microbialbiomass by predators and grazers; McArthur, 2006),dynamic (e.g. due to desiccation–rehydration cycles ornutrient limitation), and/or transient (Tables S1 and 7).As is true for open habitats of plants (Anderson, 1952),open habitats of microbes can also become closed ifthey becomes water-constrained or otherwise resource-depleted; and/or the microbial community reaches station-ary phase (Paul et al., 2006): and these changes may beaccompanied by – or even a consequence of – dominationby weed species. Environments can even progress tobecome sterile; for example those with high ethanol con-centrations (Hallsworth, 1998; Pretorius, 2000). However,a dualistic concept of open habitats on the one hand andclosed habitats on the other would be simplistic; in realitythere is a seemless continuum between the two extremesof fertile but uncolonized and hostile/uninhabitable envi-ronment. Habitats with a favourable water activity for mostbacteria (� 0.94) and high concentrations of carbon andnitrogen substrates such as milk, cheese and crushedpeanuts (Table S1) typically progress to a closed condition(and are dominated by lactic acid bacteria), as do mosthigh-sugar habitats (Table S1). A number of the openhabitats listed in Table S1 that are resource-rich, andstressful, temporally or spatially heterogenous, and/orrequire saprotrophic nutrition were dominated by Pichia(e.g. moist barley grains; salted fermenting olives) orAspergillus species (e.g. decomposing leaf litter, sugar-cane juice). The stress biology, energy-generating capa-bilities and antimicrobial activities of these speciesundoubtedly contribute to their success (Tables 3 and 6).

Ecophysiological classification

Microorganisms have been previously categorized basedon the way in which their phenotype impacts ecologicalbehaviour: as autotrophs and heterotrophs; generalistsand specialists; r- and K-strategists, aerobes and anaer-obes; copiotrophs and oligotrophs; fast and slow growers;and extremophiles and mesophiles (see Table 4 and S2).The definition of microbial weeds is qualitatively distinctfrom that of other microbial groups (see Table S2): onlyweeds are characterized by their ability to dominate com-munities and the associated/underlying biology (Tab-les S1, 2–6 and S2) and it is only weeds that are linked viatheir ecology and evolution with open habitats (Tables 1,S1, 3 and S2). The biology and ecology of microbialweed species cuts across established groupings of



microorganisms (i.e. the former does not represent a par-allel category; see Table S2). Some microbes have aconsiderable number of weed traits but only rarelyemerge as dominant members of communities (e.g. Pseu-doxylaria spp., E. coli and M. smegmatis; see Tables S1and 3, 5 and 6). Such species serve as a reminder thatweeds and non-weeds represent two extremes of an oth-erwise continuous scale. An insightful study of Termitomy-ces ecology, for example, discusses the biology ofPseudoxylaria; a fungus that is present in Termitomyceshabitats but is typically inactive and/or present at negligi-ble cell densities (Visser et al., 2011). Pseudoxylaria couldbe ecologically disadvantaged if present in greaternumbers as termites, which can detect VOCs producedduring interactions between Pseudoxylaria and Termito-myces, remove the unwanted fungus from their Termito-myces cultures. The extant Pseudoxylaria strains therebyappear to have been selected for/have evolved a lowcompetitive ability (Visser et al., 2011). NeverthelessPseudoxylaria can occasionally emerge to dominate thesubstrate (Visser et al., 2011), a fertile open habitat con-sisting of decomposing plant material (Table S1). Non-weed species make up a loose affiliation of species thatare only linked by their poor ability to dominate commu-nities in open habitats and may not share any specificmetabolic or phenotypic traits (Table S2). We propose thatthis ‘dustbin’ group includes Synodropsis spp., Polypae-cilum pisce, Metschnikowia orientalis, Caulobacter cres-centus and Salmonella species (Table S2). Severalecophysiological classification systems that are based onmicrobial growth-phenotype and/or substrate utilization(Table S2). Microbial generalists can occupy a wide rangeof ecological niches, and typically achieve this via theability to utilize a wide range of nutrients and substrates(Table S2). Conversely microbial specialists, such asS. cerevisiae, H. werneckii and many basidiomyceteshave specific nutritional and/or physicochemical require-ments (de Fine Licht et al., 2005; Kashangura et al.,2006). Obligate extremophiles commonly occupy, and areadapted to grow optimally in, niches that are hostile to themajority of microorganisms (Table S2). There have beenrelatively few studies (and is consequently inadequateterminology) to properly describe microbes that areextremo-intolerant such as xero-intolerant species (seeTable 4), with the exception of mesophilic species thatfunction optimally at non-extreme temperatures (thoughthe term mesophiles can be used in a general sense torefer to non-extremophiles: Table S2; Gostincar et al.,2010). Non-extremophilic microbes grow optimally inphysicochemical conditions which favour metabolic activ-ity and growth of the majority of microbial species, andthis grouping includes both weed and non-weed species(Table S2). While fast-growing microbes have shortdoubling times, the vast majority of these species do not

have weed-like capabilities and are unable to out-growtheir competitors (Tables 4 and S2). It may be that rela-tively few oligotrophic microbes or K-strategists are weedspecies, although some mycobacteria do have a weedphenotype (Tables S1, 3, 5 and 6). Pseudomonas putidais generally considered to be a model r-strategist (e.g.Margesin et al., 2003) yet P. putida has an extraordinarycompetitive ability (see Tables S1 and 4–6), and maynot be the best example of an r-strategist (the latter arecharacterized by a weak competitive ability; Table S2).By contrast P. putida appears to be an exceptionalexample of a microbial weed both in terms of its cellularbiology and its ability to dominate diverse types of openhabitat.

Concluding remarks

It is irrefutable that a small minority of microbial speciesrecurrently appear as the dominant members of microbialcommunities; and we suggest here that these microbeshave shared phenotypic traits. This implies that open-habitat ecology has impacted the evolutionary trajectoriesof these microbes, and that the activities of weeds deter-mine microbial diversity in many localities within the bio-sphere. Whereas microbial weed species are not alwaysuseful to humankind (see Table 1), they make up a sub-stantial portion of the world’s biotechnology sector. Sac-charomyces cerevisiae supports global industries infermented products, biofuel, biocides (ethanol is also animportant disinfectant; McDonnell and Russell, 1999), andother white biotechnologies; P. anomala produces a sub-stantial catalogue of biotechnologically useful substancesand is employed in production of foodstuffs (see Walker,2011); lactic acid bacteria form the basis of food- anddrinks-production processes where the antimicrobial vola-tiles and organic acids that they secrete act as flavourcompounds and natural preservatives, and are used asprobiotics, and for the production of fine chemicals (Rose,1982; Steinkraus, 1983; Molly et al., 1996; Nomura et al.,1998; Tiwari et al., 2009; Randazzo et al., 2010; Bronet al., 2012); P. putida is used for the commercial produc-tion of bulk and fine chemicals, industrial biocatalysis, andas the basis of many other industrial and environmentalbiotechnologies (Kruijt et al., 2009; Puchałka et al., 2008;Hassan et al., 2011; Poblete-Castro et al., 2012); anumber of weed species, including Aspergillus spp.,P. putida and Clostridium spp. play primary roles in thetreatment or decomposition of plant matter, oil and hydro-carbons, xenobiotics in polluted soils, sludge and slurrytreatments, and other organic wastes (Tables S2 and 4;Narihiro and Sekiguchi, 2007; Timmis, 2009); andAspergillus species are used for production of foods(Rose, 1982; Tamang, 2010), fine chemicals (e.g. citricacid, secondary metabolites) and extracellular enzymes



(e.g. amylase, cellulase, pectinase and protease), forindustrial biocatalysis, and have potential for bioremedia-tion and biosorption applications (Ward et al., 2006). It isthe metabolic activities of substances that suppresspotential competitors which make S. cerevisiae, Rhodo-torula spp., P. anomala, P. putida, lactic acid bacteria andother weed species invaluable as agents of biologicalcontrol, for preventing spoilage of drinks, foodstuffs andanimal feeds (see Calvente et al., 1999; Kruijt et al., 2009;Hassan et al., 2011; Olstorpe and Passoth, 2011; Walker,2011).

Microbial weeds are also used as model systems forresearch, yet key aspects of their biology remain enig-matic. Many plant weeds have exceptional reproductionand dispersal systems (Table 1) and it remains unclearwhether microbial weed species produce more prop-agules, have superior dispersal mechanisms, or evolvedpropagules with exceptional longevity, and/or the ability togerminate over a wider range of conditions than theirnon-weed comparators. Could it be that, like plant weeds,the competitive ability of microbial weeds is enhanced byan abnormally high phenotypic plasticity and intra-specificvariability (see Table 1)? Out of the world’s plant flora ithas been estimated that only several hundred plantspecies are weeds (Hill, 1977); what percentage ofmicrobes might exhibit weed phenotypes and behaviour?Is there evidence preserved in rocks, sediments, peat,ice, or the hypersaline fluid inclusions of salt crystals thatcan shed light on the evolutionary trajectories of microbialweed species? Is there an ideal genome size forprokaryotic and eukaryotic weed species? What are theminimum/essential characteristics required to enable amicroorganism to dominate a specific habitat; can wedesign and manufacture a microbial weed via a syntheticbiology approach? Will hitherto uninvestigated microbialweeds prove to be rich sources of antimicrobial com-pounds for novel biotechnological and clinical applica-tions? Can microbial weed ecology shed light on woundmicrobiology, lead to the prevention of the microbial colo-nization of prosthetic devices, or minimize the emergenceof opportunistic pathogens? Could knowledge-basedinterventions in weed ecology enhance our ability tomanipulate and manage microbes at various levels offood-production and food-spoilage, or lead to better man-agement of environments that harbor potentially danger-ous species?

Crop plants such as sunflowers, potatoes, wheat andbarley are known to have weedy ancestors (Anderson,1952) and it is thought that the evolution of both plantweeds and crop plants has been driven by anthropogeni-cally opened habitats. We believe that open (microbial)habitats also select for the phenotypes, and therefore actas a potent driving force that determines the evolutionarytrajectories, of microbial weeds and their communities:

open-habitat ecology may therefore be worthy of recog-nition as a distinct scientific field that spans all organis-mal biology including microbiology. There is a maxim thateverything is everywhere but that the environmentselects; this implies that microbial species are every-where on Earth but that the local environment deter-mines which are able to grow (Baas Becking, 1934; deWit and Bouvier, 2006). While not necessarily untrue,this idea implies a level of passivity on the part of themicrobial cell. Yet microorganisms are inherently variableand dynamic systems with considerable genetic dexterityand phenotypic plasticity (able to both respond andadapt). Baas Becking (1934) acknowledged that cells areable to modify their extracellular environment, butmicrobes are also proactive in their manipulation of eachother. It may be that microbial weeds are the mostaccomplished examples of this.

Acknowledgements

We are most grateful to T.A. Hill (University of London,UK) for his inspirational lectures on the biology of plantweeds; and for scientific enjoyable and fruitful discussionswith E. J. Carpenter (San Francisco State University,USA), L.R. Cooke (Agri-Food and Biosciences Institute,Belfast); B.T.M. Dentinger (Royal Botanic Gardens, Kew,UK), N. Gunde-Cimerman (University of Ljubljana, Slov-enia), S. Iwaguchi (Nara Women’s University, Japan),M.-A. Lachance (University of Western Ontario, Canada),K.D. Farnsworth, I.R. Grant, J.D.R. Houghton, C.J. Law,A.L. McCann, J.W. McGrath, J. Megaw, J. P. Quinn, andJ.T. Russell (Queen’s University Belfast), J.L. Green, andA.M. Womack (University of Oregon, USA), T.J. McGenity(University of Essex, UK), T. Mock (University of EastAnglia), A. Oren (The Hebrew University of Jerusalem,Israel), I.S. Pretorius (University of South Australia, Aus-tralia), R. Santos (Laboratório de Análises of the InstitutoSuperior Técnico, Lisbon, Portugal), R.S. Singhal (Insti-tute of Chemical Technology, Mumbai, India), G.G.Stewart (Heriot-Watt University, UK), J.P. Tamang (SikkimUniversity, India), K.N. Timmis (Helmholtz Centre forInfection Research, Braunschweig, Germany), M.A.Voytek (NASA Headquaters, USA).

Conflict of interest

None declared.

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Supporting information

Additional Supporting Information may be found in theonline version of this article:

Table S1. Examples of open habitats in which specificmicrobes attain dominance.Table S2. Biology of microbial weeds compared with that ofother ecophysiological groups.



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