A taxonomic review of the genus Phaeocystis - AWIliar tubular extrusomes, a second non-colonial species from the north western Mediterranean Sea producing a lot of mucus, and a colonial

Biogeochemistry (2007) 83:3–18
DOI 10.1007/s10533-007-9087-1
REVIEW PAPER

A taxonomic review of the genus Phaeocystis

Linda Medlin · Adriana Zingone

Received: 20 October 2005 / Accepted: 22 August 2006 / Published online: 15 March 2007© Springer Science+Business Media B.V. 2007

Abstract Phaeocystis is recognized both as anuisance and as an ecologically important phyto-plankton species. Its polymorphic life cycle withboth colonial and Xagellated cells causes manytaxonomic problems. Sequence variation among22 isolates representing a global distribution ofthe genus has been compared using three molecu-lar markers. The ribulose-1,5-bisphosphate car-boxylase/oxygenase (RUBISCO) spacer is tooconserved to resolve species. The most conserved18S ribosomal deoxyribonucleic acid (rDNA)analysis suggests that an undescribed unicellularPhaeocystis sp. (isolate PLY559) is a sister taxonto the Mediterranean unicellular Phaeocystisjahnii; this clade branched prior to the divergenceof all other Phaeocystis species, including the colo-nial ones. The internal transcribed spacer (ITS)region shows suYcient variation that some spatialpopulation structure can be recovered, at least inP. antarctica. P. globosa and P. pouchetii have

multiple diVerent ITS copies, suggestive of crypticspecies that are still able to hybridize. A molecu-lar clock has been constructed that estimates thedivergence of the cold water colonial forms fromthe warm-water colonial forms to be about 30 Maand the divergence of P. antarctica and P. pouch-etii to be about 15 Ma. A short description of thecolonial stage and the Xagellated stage for eachformally recognized species is provided. Morpho-logical information is also provided on a numberof undescribed species. These include the strainPly 559, consisting of non-colonial cells with pecu-liar tubular extrusomes, a second non-colonialspecies from the north western MediterraneanSea producing a lot of mucus, and a colonial spe-cies with scale-less Xagellates found in Italianwaters. In addition, three Xagellated morphotypeswith scales diVerent from those of P. antarcticawere reported in the literature from Antarcticwaters. The picture emerging from both molecu-lar and morphological data is that the number ofspecies in the genus is still underestimated andthat cryptic or pseudocryptic diversity requires asound assessment in future research of this genus.Based on all published observations, an emendeddescription of the genus is provided.

Keywords Molecular clock · Phaeocystis antarctica · P. cordata · P. globosa · P. jahnii · P. pouchetii · P. scrobiculata ·rDNA analysis

L. Medlin (&)Alfred Wegener Institute for Polar and MarineResearch, Am Handelshafen 12, Bremerhaven, 27570, Germanye-mail: [email protected]

A. ZingoneStazione Zoologica Anton Dohrn, Villa Comunale, 80121 Naples, Italy

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4 Biogeochemistry (2007) 83:3–18

Introduction

Phaeocystis Lagerheim is a cosmopolitan bloom-forming alga that is often recognized both as anuisance alga and an ecologically important memberof the phytoplankton (Davidson 1985; Lancelotet al. 1987; Smith et al. 1991; Davidson andMarchant 1992; Baumann et al. 1994; Schoemannet al. 2005; Veldhuis and Wassmann 2005). Itsvarious life forms can make large-scale bloomsthat are often avoided by Wsh (Chang 1983) andappear detrimental to the growth and reproduc-tion of shellWsh and macrozooplankton (Davidsonand Marchant 1992) or are ichthyotoxic (Shenet al. 2004). Massive areas of pollution are createdwhen dissolved organic compounds released byPhaeocystis during declining bloom conditionsaccumulate, foam and then wash onshore (Lancelotet al. 1987). Phaeocystis is a major contributor tothe global sulphur budget by releasing substantialquantities of dimethylsulWde propionate (DMSP)(Keller et al. 1989; Baumann et al. 1993), which ismetabolized to dimethylsulWde (DMS) as the cellsare grazed or infected and lysed by viruses. It mayplay yet another important ecological role with itsproduction of ultraviolet B (UV-B)-absorbingcompounds (Marchant et al. 1991; Davidson andMarchant 1992).

Phaeocystis has a polymorphic life cycle withboth colonial and Xagellated cells (Kornmann1955; Whipple et al. 2005). The colonial stage,with cells very loosely interconnected andenclosed in a thin skin (Hamm et al. 1999), ismost easily recognized, although some speciesmay form mucilaginous colonies or do not seemto have a colonial stage. Thousands of cells canoccur in a colony that may reach 2 cm in diameter(Jahnke and Baumann 1987; Verity et al. 1988;Rousseau et al. 1994; Davidson and Marchant1992). Colony sizes of 3 cm or more have beenreported in blooms from China (Shen et al. 2004).The diYculty in assigning a speciWc name to thecolonial stage has caused much taxonomic confu-sion. Flagellated cells have two parietal chlorop-lasts and two Xagella, which may be equal orunequal in length and heterodynamic. A shorthaptonema is present between the two Xagella,which may or may not have a swollen end. TheXagellated cells may be naked or have two layers

of diVerent shaped organic scales. Some Xagel-lated cells also produce groups of Wlaments, whichare extruded from the cell and assume a charac-teristic pattern.

The genus was erected by Lagerheim in 1893 toaccommodate the colonial stage of an algadescribed originally as Tetraspora poucheti byHariot in Pouchet (1892). Phaeocystis pouchetii(its correct orthography) occurs in cold watersand in its globular, lobed colonies, cells arearranged in packets of four (see Jahnke andBaumann 1987 for illustrations). Phaeocystisglobosa was described by ScherVel (1900) fromtemperate waters and forms spherical colonies withcells arranged homogeneously within the colony(Jahnke and Baumann 1987), whereas olderstages can assume distorted pear shapes (Bätjeand Michaelis 1986). Early workers separatedP. pouchetii and P. globosa based on diVerentdistributions and colonial morphologies untilKornmann (1955) doubted the diVerentiationbetween the two species. From his life-cycle studies,he considered that P. globosa cell types appearedto be juvenile forms of P. pouchetii. Since thatreport, colony morphology has been judged anunreliable speciWc character.

Sournia (1988) reviewed the diagnosticfeatures of Phaeocystis, and discussed the reliabilityof the nine valid species published since the lastcentury. He discarded two species from the genus,P. fuscescens (Braun) De Toni and P. giraudyi(Derbès and Solier) Hamel, because they did notWt the genus and probably not even the class char-acteristics. The descriptions of four species, twofrom cold waters, P. antarctica Karsten andP. brucei Mangin, and two from temperate waters,P. amoeboidea Büttner and P. sphaeroidea Bütt-ner, were all judged as very superWcial. The poorillustrations and unlikely features, including onechloroplast per cell and no haptonema (Büttner1911), were probably the reasons why the twotemperate species have never been mentionedagain in the literature. For similar reasons the twoAntarctic species were reported rarely and notstudied again. As for the two most frequentlyrecorded species, P. pouchetii (Hariot in Pouchet)Lagerheim and P. globosa ScherVel, they hadbeen studied in more detail yet no element wasavailable to keep them separate. Therefore Sournia

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Biogeochemistry (2007) 83:3–18 5

suggested that the name P. pouchetii or, better,P. cf. pouchetii should have been used for thecolonial Phaeocystis species pending new infor-mation. The only other reliable species was Phae-ocystis scrobiculata Moestrup, described withmodern methods but known only from the Xagel-lated state (Moestrup 1979). Without convincinginformation on the diVerentiation betweenP. pouchetii and P. globosa (see paragraph below),most marine ecologists until the mid 1990s fol-lowed Sournia’s advice and reported Phaeocystiscolonies as P. pouchetii (the older name) or asPhaeocystis sp. to avoid confusion.

Baumann and Jahnke (1986), Jahnke andBaumann (1986, 1987) and Jahnke (1989) regardedthis as over-simpliWcation. Their observations oncolony shape maintenance in long term cultureshowed that both juvenile and older stages ofP. globosa and P. pouchetii were distinct and thesedata supported the recognition of the two entitiesas separate species. Also, detailed studies of thetemperature and light tolerances suggested sepa-ration at the species level. P. globosa was a tem-perate species and P. pouchetii was a cold-waterform. A third, unnamed colonial species fromAntarctic waters was recognized by Baumannet al. (1993), which had a combination of featuresof P. globosa and pouchetii, as suggested earlierby Moestrup and Larsen (1992). The coloniesresembled those of P. globosa (Larsen andMoestrup 1989), whereas temperature tolerancewas similar to that of P. pouchetii. Notably, strainsfrom the Antarctic had diVerent pigment spectra(Buma et al. 1991; Vaulot et al. 1994) and DNAcontent (Vaulot et al. 1994). First indications thatfurther undescribed species could exist were pro-vided by Pienaar (1991, 1996) who illustrated aPhaeocystis Xagellate with cup-shaped scales fromSouth African waters suggesting it was a new spe-cies but not publishing a formal description.

To resolve the species issue in Phaeocystis, amolecular analysis of various clones was begun(Lange 1997). Medlin et al. (1994) were the Wrst topropose that P. globosa and P. pouchetii were sep-arate species based on genetic evidence. They alsoshowed that colonial Phaeocystis from the Antarc-tic was genetically distinct from the other two spe-cies. They resurrected the species P. antarcticadescribed by Karsten (1905) for the colonial

isolates previously termed P. globosa or pouchetiifrom these waters. Zingone et al. (1999) addedtwo more species to the genus, P. cordata andP. jahnii, but these were basically unicellular spe-cies, although the latter species could make simpleclusters of cells that could be termed colonial. Inthis review we summarize the molecular and mor-phological information available to date for Phae-ocystis species and provide evidence that a highdiversity is still hidden in the genus.

Molecular analysis

A global distribution of the prymnesiophytegenus Phaeocystis was compared using nuclear-encoded 18S rDNA genes and two non-codingregions, the ribosomal DNA internal transcribedspacer 1 (ITS1) separating the 18S rDNA and5.8S rDNA genes and the plastid ribulose-1,5-bis-phosphate carboxylase/oxygenase (RUBISCO)spacer Xanked by short stretches of the adjacentlarge and small subunits (rbcL and rbcS) (Langeet al., 2002). The RUBISCO spacer regions werehighly conserved and generally uninformativeamong all Phaeocystis strains (Lange et al. 2002).The 18S rDNA analysis suggests that an unde-scribed unicellular Phaeocystis sp. (isolatePLY559) is a sister taxon to the occasionally colo-nial Mediterranean P. jahnii with which it forms aclade that diverges at the same time from a cladewith all other Phaeocystis species, including thoseforming typical colonies wrapped in a skin(Fig. 1). In this latter clade, the unicellular P. cor-data diverges before the colonial ones, which canbe divided into a cold-water complex (P. pouch-etii from the Arctic and P. antarctica from theAntarctic) and a warm-water complex consistingof P. globosa. Thus, all of the variation seen ear-lier using morphological and physiological criteriahad a strong genetic basis and separation at thespecies level was warranted for all colonial spe-cies originating from major climatic regions, i.e.,the Arctic, the Antarctic and temperate/tropicalregions.

In contrast, ITS1 exhibited substantial inter-and intra-speciWc sequence divergence andshowed more resolution among the strains(Fig. 2). Markedly diVerent copies of the ITS1

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region were found in P. globosa even amongcloned DNA from a single strain, suggesting thatit is a species complex composed of at least threespecies. This observation was also supported bydiVerent DNA content among diVerent clones ofPhaeocystis (Vaulot et al. 1994). Multiple copiesof the ITS1 were also found in a single strain of P.pouchetii, suggesting that this is also a speciescomplex. These species complexes would appearstill to be able to interbreed with one anotherbecause multiple diVerent haplotypes from diVer-ent clades can be found within a single strain.Similar Wndings of multiple haplotypes beingpresent in known hybrids of Xowering plant spe-cies are quite common (Chase et al 2003) and it isknown that in some hybrids of Xowering plants,the hybrid can loose one of the parental haplo-types in as few as 12 generations (Bateman, pers.com.) However, among nine P. antarctica strains,only one type of ITS1 haplotype was found perstrain, although it was variable among the strains.Using the branching order in the ITS1 tree(Fig. 3) we have attempted to trace the biogeo-

graphic history of the dispersal of strains in Ant-arctic coastal waters. We see that the Wrstdivergence among the Antarctic clade is strain SK22, which was isolated from the Antarctic circum-polar current (ACC). The second divergence is astrain from Prydz Bay (T4-2) and this is then fol-lowed by a nearly simultaneous divergence of theremaining strains. Among these divergences is acluster of strains from Prydz Bay (DE2, A1-3 andT9-1). The other divergence includes strainCCMP 1374 from the Ross Sea and two Phaeo-cystis strains from the Weddell Sea (SK 20, SK23) (Fig. 3) and Wnally strain D4-5 from PrydzBay, which shares a last common ancestor withthe Weddell Sea strain SK 23, as the Wnal clusterto diverge among the Antarctic strains. Popula-tions of P. antarctica within the continentalboundary water masses appear to be well-mixedbecause currents move around the Antarctic con-tinent rather quickly and may eVectively act as abarrier to signiWcant population structure. StrainSK 22 isolated within the ACC, however, isclearly diVerent. An earlier hypothesis, proposed

Fig. 1 Maximum-likeli-hood phylogeny (fastD-NAml) of 17 Phaeocystis species/strains and other prymnesiophytes inferred from 18S rDNA. The class Pavlovophyceae was used as outgroup. Bootstrap values are placed on the nodes that are identical from ML/NJ/MP analyses. The scale bar corresponds to two base changes per 100 nucleotides. Redrawn from Lange et al. (2002)

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from rDNA data (Medlin et al. 1994), that ances-tral populations in the Antarctic gave rise to pres-ent day P. antarctica and P. pouchetii populationsappears to be supported by ITS1 analysis of thecold-water Phaeocystis strains. P. antarctica andP. pouchetii, both polar, are more closely relatedto one another than either is to the cold and warmtemperate to tropical populations of present-dayP. globosa. This suggests that dispersal did notoccur from present-day warm-water populationsinto present-day cold-water populations but thatgene Xow has occurred from pole to pole acrosstropical oceans. Arctic P. pouchetii populationsthus probably arose by a dispersal event from thesouth to the north during colder climate periodsthat allowed populations to survive the crossingof equatorial waters, as has been documented forother organisms (Crame 1993; Darling et al. 2000,2004; Montresor et al. 2003). A subsequent warm-

ing event will then isolate the two polar popula-tions. Evidence for this can be found in a study ofAntarctic surface-water temperatures since theCretaceous (Crame 1993, Fig. 4c).

If we follow the branching order in Fig. 1, wehypothesize the following scenario: Phaeocystislikely originated as a warm-water genus becauseWrst divergences in our tree are warm-water spe-cies. Ancestral populations in the Antarctic werederived from ancestors of the present-day warm-water species, after being isolated in Antarcticwaters. The opening of the Drake passage and theformation of the Antarctic circumpolar current(ACC) are the most likely geological events thatcould have isolated populations in the Antarcticto separate them from warm-water ancestors. Itcan be inferred from Fig. 3 that presumed descen-dants of these warm-water ancestors were Wrstentrained in the ACC because these are the Wrst

Fig. 2 Maximum-likeli-hood phylogeny of the ITS regions showing the multiple sequences from a single strain of P. globosa and P. pouchetii. Each diVerent sequence comes from a diVerent bacterial vector clone. All haplo-types from one strain of Phaeocystis are connected by the arrows. P. antarc-tica exhibited a single se-quence per strain and these are collapsed into a triangle. Redrawn from Lange et al. (2002)

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divergences. Some of these ancestral populationsmust have been transported northward and acrossthe Equator shortly after the Drake passageopened because the P. pouchetii populations aresister to the P. antarctica populations. The ACCtoday encircles the Antarctic continent every1–2 years. Water is entrained from this currentinto the major gyres of the continental water masses(Treshnikov 1964). Using the branching order in

Fig. 3 we can trace the dispersal of the clonesfrom the ACC, although the bootstrap supportfor the branching order is weak to strong amongthe clades. The Wrst entrainment with a bootstrapsupport of 99% appears to be into Prydz Baybecause strain T4–2 isolated from this bay is theWrst divergence in our tree. These populationsthen established themselves in the Eastern Ant-arctic in Prydz Bay. Subsequent divergences inthe tree indicate that populations were thenentrained into the Ross Sea and almost simulta-neously they were entrained into the Weddell Sea(bootstrap support 54%). Both isolates from theWeddell Sea were the last to diverge before thepopulations were again entrained back into PrydzBay from populations in the Weddell Sea becauseisolates from this bay are some of the last diver-gences in the tree (bootstrap 54%). The distribu-tion of these isolates in this fashion follows thepredominant current patterns of surface waters inthe Antarctic today. What we do not know is howdiVerent the surface-water circulation was 30 Mabefore the ACC was established.

Other studies have also shown the eVect ofmixing on the homogenization of the geneticstructure of Antarctic populations. Krill specieswithin the Antarctic continental water masses arevery similar as documented by both mtDNA(Patarnello et al. unpubl.) and isozyme analysis(Fevolden and Schneppenheim 1989). The mtDNAstudy also suggested that the formation of theACC eVectively isolated krill species in Antarcticwater masses from those north of the ACC.Calculation of the time of divergence betweenspecies groups found either side of the ACC coin-cided with the timing of the ACC, approximately30 Ma. Thus, the molecular data is consistent withour hypothesized historical biogeographic recon-struction of the distribution of Phaeocystis basedon the circulation patterns developed with theformation of the ACC.

Molecular clock

A molecular clock has been constructed from our18S rDNA tree and calibrated with fossil datesfrom the haptophyte coccolithophorid species(Fig. 4). Our molecular clock calculations indicate

Fig. 3 (a) Locations of the strains of P. antarctica used inLange et al. (2002). The location of diVerent clades is indi-cated by the diVerent patterns in the large circles and cor-respond to those clades in (b). Prydz Bay locations inE. Antarctica are slightly displaced for visual clarity. (b)Maximum-likelihood tree inferred from ITS1 sequencesfrom P. antarctica with P. pouchetii as outgroup. Bootstrapvalues are placed at the nodes from a maximum likelihoodanalysis (100 replicates) a neighbor-joining analysis(500 replicates) and a maximum parsimony analysis(500 replicates). The scale bar corresponds to two changesper 100 nucleotide positions. Redrawn from Lange et al.(2002). Map of Antarctica redrawn from Olbers et al.(1962)

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Fig. 4 Calculation of a molecular clock. (a) The ml treeshown in Edvardsen et al. (2000) has been linearized(Kooistra and Medlin 1996) so that all rates of evolutionare the same. Fossil dates from coccolithophore taxa areplaced on nodes where these taxa have their Wrst appear-ance in the fossil record (open circles on tree). (b) A regres-

according to Kooistra and Medlin (1996). From this regres-sion line we have extrapolated the divergence of the warm-and cold-water Phaeocystis (Y) and the divergence ofP. pouchetii from P. antarctica (£) (solid circles on tree).(c) Temperature of Antarctic surface waters since the Cre-taceous with the molecular tree plotted proportional to the

Oolithotus fragilis

Algirosphaera robusta

Umbilicosphaera sibogae var. foliosa

Dicrateria sp.

Calyptrosphaera sp. 1

Diacronema vlkianum

Hymenomonas globosa

Calyptrosphaera radiata

Ochrosphaera neapolitana

Platychrysis simplex

Hymenomonas coronata

Calcidiscus leptoporus intermediate

Cruciplacolithus neohelis

Imantonia rotunda

Chrysochromulina minor

Chrysochromulina hirta

Chyrsochromulina cymbium

Pleurochrysis carterae

Pleurochrysis carterae var. dentata

Pleurochrysis elongata

Isochrysis litoralis

Pavlova gyrans

Pseudoisochrysis paradoxa

Pleurochrysis gayraliae

Umbilicosphaera hulburtiana

Scyphosphaera apsteinii

cf. Jomonlithus littoralis

E. huxleyi /G. oceanica

Phaeocystis jahnii

Fucus

Coccolithus pelagicus big

Helicosphaera carteri var carteri

Chrysotila lamellosa

Pavlova lutheri

Pavlova virescensExanthemachrysis gayraliaeRebecca salina

Pavlova sp. CCMP1416

OLI 51059CCMP 1204

CCMP 1404Imantonia sp.

OLI 26041

Calcidiscus leptoporus large

Unidentified coccolithophorida

Pleurochrysis sp.

Pleurochrysis sp.

Coronosphaera mediterraneaSyracosphaera pulchra

OLI 510521

Chyrsochromulina parkaePhaeocystis PLY 559

Phaeocystis cordata

Phaeocystis globosa

OLI 51080

OLI 51004

OLI 51076OLI 26047

OLI 16010

Chrysochromulina kappa

Chrysochromulina simplexChrysochromulina leadbeateri

Chrysochromulina herdlensis

Prymnesium parvum

Chrysochromulina polylepis

Prymnesium calathiferum

Chrysochromulina campanuliferaChrysochromulina strobilus

OLI 16029OLI 51102OLI 26017OLI 16108

Chrysochromulina cf. ephippiumChrysochromulina throndsenii Chrysochromulina rotalisChrysochromulina parvaChrysochromulina spinifera

Prymnesium faveolatum

Platychrysis pigra

Prymnesium tunis

Chrysochromulina chiton

Chrysochromulina brevifilum

Phaeocystis antarcticaPhaeocystis pouchetii

Reticulosphaera japonensisPleurochrysis sp.

Distance to node

MA

0

50

100

150

200

0,2 0,4 0,6 0,8 1 1,2 1,4

B1

C1

A

B2

YX

(a)

(b) (c)

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sion of branch lengths against fossil dates has been performed time and the temperature, redrawn from Crame (1993)


that the warm-water Phaeocystis species divergedfrom the cold-water species approximately 30 Ma,which coincides with the time that the Drake pas-sage opened and the ACC system was formed.This would have eVectively isolated ancestralpopulations in the Antarctic suYciently to allowthem to speciate from their warm-water ances-tors. The separation of P. pouchetii from P. ant-arctica is approximately 15 Ma, which coincideswith a major warming event in the world’s oceansat this time (Fig. 4). Before this time populationsmust have been able to cross the equator from thesouth to the north because water temperatureswere cool enough to allow survival, but thiswarming event separated the two polar popula-tions to allow them to diverge into the two specieswe have today at the poles. Similar results havebeen found for foraminfera (Darling et al. 2000,2004).

Thus molecular data have deWned our specieswell and suggest which species are likely to becomposed of cryptic species. We detail belowbasic descriptions of each of the formallydescribed species and provide some indication asto other undescribed species where this informa-tion is known.

Formally described species

An overview of the validly published taxa thathave been re-examined in recent years is pre-sented in the following. These include specieslisted in the genus in its most recent review (Sour-nia 1988) and new species described after thatdate, with the exception of three taxa that havenot been studied since their description, P. amoe-boidea Büttner, P. sphaeroidea Büttner andP. brucei Mangin. The Wrst two of these do not havefeatures characteristic of the genus, much thedivision Haptophyta, so it is likely that only thelatter species may still be a valid species of Phaeo-cystis. The main distinctive characters of the spe-cies included in this section are summarized in atable in Jacobsen (2002).

P. pouchetii (Hariot in Pouchet) Lagerheim(Pouchet 1892) forms cloud-like colonies with cellsin packets of four (Fig. 5a). Molecular data suggestthat this is a species complex but here very few

strains have been examined with molecular tech-niques so this is only a very preliminary suggestion.

Flagellated stages of P. pouchetii (Fig. 6a)were the subject of recent morphological studies(Jacobsen 2000, 2002). Cells are rounded, with anaverage diameter of 5 �m. The Xagella are equalin length, ca 11 �m, and heterodynamic. Thehaptonema is extremely short, 1–2 �m, with aslight swelling, and is not easily seen with lightmicroscopy. Body scales are of two types: almostcircular Xat plates, 0.24 £ 0.25 �m, with raisedrims, forming an external layer and smaller ovalplates with slightly inXexed rims, 0.19 £ 0.15 �m,underneath the larger scales. Both types of scalesshow thin radiating ridges. Filaments (up to30 �m) arranged in groups of Wve with the typicalpentagonal proximal structure are seen outsidethe cells, or are coiled up in vesicles under the cellsurface. The presence of silica is reported in theseWlaments (Jacobsen 2002). The ultrastructure issimilar to that of P. globosa (Parke et al. 1971)and of the other Phaeocystis for which this infor-mation is available (Zingone et al. 1999), with thenucleus located posteriorly, the two chloroplastswith the embedded pyrenoids, and the Golgi bodybetween them. This cell stage can be infected byviruses (Jacobsen et al. 1996).

P. globosa ScherVel (ScherVel 1900) formsglobular colonies with the cells evenly distributedthroughout the colony (Fig. 5b). Molecular dataand DNA content suggest that this is a complex ofup to three or four cryptic species, but to date nomorphological investigations exist to support this.

Flagellated stages of P. globosa (Fig. 6b, c)were described for the Wrst time by Parke et al.(1971) under the name of P. pouchetii, at the timewhen these two species were considered as stageswithin the life cycle of the same species. Cells are3–6 �m, more frequently between 3 and 4.5 �m.The two Xagella and the haptonema emerge froma depression in the cell body. Flagella are equal inlength, 1.5£ the cell length, and heterodynamic.The haptonema is a quarter to a third the lengthof the Xagella. It is stiV and has a clear distal swell-ing. The haptonema is easily seen in live cells,where it is directed forward while cells move.Body scales show all radiating ridges on both sur-faces and are of two types: almost circular Xatplates, 0.18 £ 0.19 �m, with raised rims, forming

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an external layer and smaller oval plates,0.10 £ 0.13 �m, with strongly inXexed rims,underneath the larger scales. The ultrastructure istypical for the genus, with two golden-brownchloroplasts, with internal fusiform pyrenoids,and some refringent vesicles probably includingstorage products. The nucleus is posterior,whereas the Golgi body, with a high number ofstacked cysternae, is seen in the space betweenthe chloroplasts and the nucleus. The Xagellarbases have typical distal and proximal plates inthe transition zone. One of the two clonesobserved by Parke et al. (1971) (clone 147) formslong Wlaments (up to 20 �m) in groups of Wvewhen discharged outside, with the proximal endsarranged in a very typical pentagonal structure,surrounded by a faint vesicle with a pore in thecentre. In the cells, the undischarged threads arefound within a vesicle under the cell surface.Chrétiennot-Dinet et al. (1997) showed that theseWlaments contain alpha-chitin.

P. antarctica Karsten (Karsten 1905) is theleast known Phaeocystis from the morphological

point of view. It also forms globular colonies withcells randomly distributed under the colony sur-face (Fig. 5c, d). These colonies can become quitedistorted and elongated with age.

Flagellated stages of P. antarctica (Fig. 6d)have received very little study. Only one illustra-tion of scales from an Antarctic Phaeocystis wasavailable (Larsen and Moestrup 1989), showingoval scales of two diVerent sizes (0.27 £ 0.19 �mand 0.18 £ 0.14 �m, respectively). Recently, threediVerent morphs have been illustrated from Weldmaterial from the Antarctic having scales that arediVerent in size as compared to those shown byLarsen and Moestrup and having a haptonemawithout a bulge on its tip (Marchant et al. 2005,Figs. 6f, 7d–f). Scales of still diVerent sizes havebeen detected in Xagellated stages obtained fromthe isolation of colonies, which are phylogeneti-cally close to SK 22 (Zingone and Montresor,unpublished). The molecular data published todate are derived only from colonial stages or fromXagellate stages that were originally colonial.There is only a single type of ITS sequence pres-

Fig. 5 Light microscopic micrographs of colony stages ofPhaeocystis. (a) P. pouchetii, (b) P. globosa, (c) P. antarc-tica, young colony, (d) P. antarctica, older colony, (e) P.

jahnii, (f) Phaeocystis sp.2 (a, b) taken from http://www.jo-chemnet.de/Wu/OCB3043_21.html Scale bar = 100 �m

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Fig. 6 Light microscopy (LM), transmission electronmicroscopy (TEM) and scanning electron microscopy(SEM) micrographs of Xagellated stages of Phaeocystis. (a)P. pouchetii, TEM, (b) P. globosa, SEM, (c) P. globosa,LM, (d) P. antarctica, LM, (e) P. jahnii, TEM, (f) Phaeocys-tis sp. from Antarctic waters TEM, (g) Phaeocystis sp. 3,SEM, (h) P. cordata TEM, (i) P. cordata, star-like pattern

in the center of the Wve-Wlament structure, TEM, (j) P. cor-data, SEM. (a) from Jacobsen (2002), (c) taken by AnnaNoordeloos, (d) taken by Dr. P. Assmy, (f) from Scott andMarchant (2005), (e, h, i) from Zingone et al. (1999), (b)and (g) from Vaulot et al. (1994). Scale bar = 1 �m on (a, b,g) Scale bar = 10 �m on (c, d) Scale bar = 2 �m on (e–j)Scale bar = 0.3 �m on (i)

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ent in each strain in contrast to the multiple ITSvariants in P. pouchetii and P. globosa, whichstrongly suggests that colonial Phaeocystis from theAntarctic are not a species complex. The similarity

among ITS sequences from Antarctic strains indi-cates that they could be all a single species,whereas these new unicellular morphs in Weld sam-ples may belong to species as yet uncultivated

Fig. 7 LM, TEM and SEM micrographs of Xagellated stag-es of Phaeocystis. (a) Phaeocystis sp. 1 (PML 559), LM, (b)Phaeocystis sp. 1 (PML 559), SEM, (c) Tip of the tube-likestructure ejected from Phaeocystis sp. 1 (PML 559), TEM.(d–f) Morphs 1, 2, 3 of P. antarctica, (g) Wlaments of P.

scrobiculata, (b, c) taken by Gandi Forlani, (d–f) from Scottand Marchant (2005). (g) From www.marbot.gu.se/SSS/others/Phaeocystis_scrobiculata.GIF. Scale bar = 10 �m on(a) Scale bar = 2 �m on (b), (g) Scale bar = 0.5 �m on (c–f)

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(Fig. 7d–f). Alternatively, diVerent Xagellate mor-photypes could belong to diVerent sub-clades inthe P. antarctica-clade. All this information indi-cates a high morphological diversity and suggeststhat there might be more than one species presentin Phaeocystis from the Antarctic. Parallel mor-phological investigations are warranted on strainsbelonging to distinct P. antarctica sub-clades.

P. jahnii Zingone (Fig. 5e) forms colonies verydiVerent from all other Phaeocystis colonies(Zingone et al. 1999). These are loose aggregatesof non-motile cells embedded in a sticky mucilag-inous matrix probably of polysaccharide nature,with no external layer nor a deWnite shape. In cul-ture material the colonies may form wide sheetswith margins at times sticking to the cell tube.Colonial cells range from 6 to 8.5 �m and have 2–4 chloroplasts.

Flagellated cells of P. jahnii (Fig. 6e) arerounded, 3.5–5 �m diameter, with Xagella of mark-edly unequal length (8.5–12 �m and 5.5–6.5 �m,respectively). The haptonema is relatively long(3–4.5 �m) and without a marked bulge at theend. As compared to the other Phaeocystis spe-cies, scales are thinner and more delicate, with avery faint radiating pattern lacking in the centralpart of the scale. The larger scales (0.35 £ 0.28 �m)do not have an upraised rim, whereas the smallerunderlying scales (0.18 £ 0.14 �m) have thetypical inXexed rim. A refringent yellow-orangebody is often seen in the live cells in the spacebetween the chloroplasts. Filaments have notbeen observed in this species.

P. cordata Zingone et Chrétiennot-Dinet(Fig. 6h–j) occurs only as single cells which aretypically triangular, heart-shaped or oval, some-what Xattened, with a deep Xagellar depressionand more or less pointed antapical end (Zingoneet al. 1999). The average size is 3–3.5 �m long,3–4 �m wide, and ca. 2.5 �m thick. The two Xagellaare slightly subequal, 5.5–7.5 and 4.5–6 �m length,respectively. The haptonema is very short(2.2–2.5 �m) and hardly visible in light micros-copy, with a bulging end observed in the electronmicroscope. Cells generally swim with the Xagel-lar pole directed backwards, and the two Xagellastraight, completely hiding the haptonema. Cellsrotate around their longitudinal axis while mov-ing. Rarely cells are seen moving with the Xagellar

pole forward. Both larger and smaller scales areoval, 0.25 £ 0.18 �m and 0.18 £ 0.13 �m, respec-tively. The larger scales have upraised rims and aslight central knob, and form the external cellinvestment. The smaller scales have inXexed rimsand form an inner layer adjacent to the plasma-lemma. The Wlaments are seen in disk-like vesi-cles underneath the cell surface (up to three in acell) or discharged, with the typical Wve-ray starpattern (Fig 6i). Ultrathin sections show the twoXagella and the haptonema inserted along a linethat is transversal to the plane crossing the plast-ids. Comparable information is not available forother species yet. The internal microanatomy issimilar to that of the other species of the genus.

P. scrobiculata Moestrup (Fig. 7g) wasdescribed from Weld material collected in NewZealand waters (Moestrup 1979) as a unicell.There is no evidence that it makes colonies norany molecular work has been done on it. Its cellsare 8 �m in diameter with two types of scales,0.6 £ 0.45 �m and 0.19 £ 0.21 �m in size. Bothtypes of scales are structureless on the dorsal side,but with ridges radiating from a plain centre onthe ventral side. Its Xagella and haptonema aretwice the length found in P. globosa and thescales are about two times larger. Another distin-guishing feature is the Wlaments that it produces,which are in groups of nine (eight pairs and onesingle), in contrast to the production of Wve singleWlaments from the other species that produce Wla-ments (Fig. 7g). The centre pattern of the Wla-ments is rather irregular and does not form thecharacteristic star shape in the middle. Filamentsarranged with the same pattern have also beenfound in Australian waters (HallegraeV 1983) andin the Mediterranean Sea (Zingone et al. 1999).However, scales were smaller in both Australianand Mediterranean specimens, which suggests apossible higher diversity to be explored withinthis taxon as well.

Undescribed species

In addition to the species described in the litera-ture, a number of taxa ascribed to Phaeocystis thatare currently under morphological and molecularinvestigation are presented in the following.

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Phaeocystis sp. 1 (PML 559) (Fig. 7a–c) seemsonly to be present in single cells. The two Xagellaare 8.5–12 �m and 5.5–6.5 �m, respectively. Thehaptonema is 3–4.5 �m long, without a bulge atthe end. The larger scales are similar to those ofP. cordata, though larger (ca. 0.35 £ 0.22 �m),with thick upraised rim and a central knob.Smaller scales (0.25 £ 0.17 �m) have inXexedrims. An unusual feature of this species is that itproduces tube-like structures with peculiar endsthat are ejected from the cell. These bodies maybe present in number of 5–7 per cell (Fig. 7b) andleave a large depression once extruded. Manybenthic stages are formed as the culture ages andit is likely that the tube-like bodies help to attachthe cells to the substrate.

Phaeocystis sp. 2 (Fig. 5f) is the only Phaeocys-tis so far cultivated from the Mediterranean Seathat has been shown to form typical colonies ofspherical shape (Zingone, Borra, Forlani and Pro-caccini, in preparation). The Xagellates have anirregular shape, with pronounced shoulders at theXagellar pole. The Xagella are markedly unequalin length, the haptonema has no bulging end. Noscales were ever detected on the cell surface, norany kinds of Wlaments. 18S analyses demonstratethat this taxon belongs to the P. globosa clade,although it diVers by nine base pairs, a diVerencethat is comparable to that between P. pouchetiiand P. antarctica. ITS sequence is unalignablewith those of those available for the otherP. globosa strains.

Phaeocystis sp. 3 (Fig. 6g) includes strains iso-lated from the North-Western Mediterranean Sea.Being single-celled and similar to P. cordata inscale morphology, it was preliminarily attributedto the latter species (as strains MEDNS2 andMEDNS3 in Zingone et al. 1999), but it has mor-phological diVerences that were initially unappre-ciated. As compared to P. cordata, Phaeocystis sp.3 is somewhat larger, has a rounded body, shorterXagella and the larger body scales are almost cir-cular rather than oval. Preliminary molecular anal-ysis has placed it within the P. globosa complex.

Clearly, morphological details of the speciesencountered in recent years fall outside of theoriginal description of the genus Phaeocystis,therefore we feel it necessary to emend the genusdescription as follows:

Phaeocystis Lagerheim 1893, Zingone andMedlin emended.

Motile cells with two more or less equal Xagellaand a shorter non-coiling haptonema; 1–4 parietalchloroplasts; cell body often covered with Xatscales of two diVerent sizes. Ejectile organellesknown for several species. Complex life cyclesinvolving the formation of non-motile stages, notknown for all species. Non-motile cells usuallywithout appendages and scales, either single orarranged in spherical, lobed, sheathed or irregulargelatinous colonies; if appendages present, usu-ally shorter or incomplete.

Outlook

From the observations we have to date, includingWeld and cultured material and molecular data, itis clear that we have come a long way from just10 years ago, when we had only one species ofPhaeocystis: P. globosa with a cosmopolitan dis-tribution. We now have a much clearer picture ofthe species in the genus and their distribution.However Phaeocystis still holds many mysteries.Clearly, there are more species of Phaeocystisthan presently formally recognized. Some of theseare morphologically distinct, whereas othersrequire further research to assess whether theyare cryptic species or, rather, they are morpholog-ically distinct at least in some stages of their lifecycle. New avenues of molecular and morphologi-cal investigation concern the taxa known onlyfrom Weld material, such as the three morpho-types of P. antarctica, and the as yet unculturedand rare P. scrobiculata, or the Xagellate withcup-shaped plates from South African waters(Pienaar 1991, 1996). As Xagellate stages appearto be more widespread and diverse as comparedto colonial stages, material to study should begathered through speciWc cultivation techniques(e.g., serial dilution techniques). Whereas thefunction of the thin Wlaments has not been fullyclariWed, the role of the peculiar extrusomesfound in PLY 559 is even more diYcult to under-stand. Presumably these are diVerent attachmentmechanisms, but they could also be involved inpotential overwintering stage formation (Gäbbleret al. unpublished observations). The molecular

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tools that have been used so far have signiWcantlycontributed to delineate Phaeocystis species.What remains to be clariWed is the genetic diver-sity within the major species and how this diver-sity changes in time and space, which will requirethe set up of new high-resolution methods (seeGäbbler et al. (2007)) for the latest developmentsin population genetic analysis of Phaeocystis).This information, coupled with a better circum-scription of species, is the prerequisite for signiW-cant advancements in the understanding of theecology of one of the key players of the worldocean’s plankton.

Acknowledgements Dr. Philipp Assmy kindly providedphotographs of P. antarctica. Gandi Forlani provided pho-tographs of Phaeocystis sp. 1 (PML 559). Photographs tak-en from Fig. 5.2 from Scott and Marchant (2005) werereproduced with permission from F.J. Scott and H.J.Marchant (Eds), Antarctic Marine Protists 258, (2005),Copyright Australian Biological Resources Study, AustralianAntarctic Division and Andrew Davidson. Figures repro-duced from ‘Morphology, relative DNA content andhypothetical life cycle of Phaeocystis pouchetii (Prymnesi-ophyceae); with special emphasis on the Xagellated celltype’ by Jacobsen (2002) from Sarsia, www.tandf.no/sarsia,2002, 87: 338–349, by permission of Taylor and Francis AS.Figures 2a, g in Vaulot et al. (1994) and Fig. 6, 9, 32 inZingone et al. (1999) were reproduced with permission ofthe Phycological Society of America. This review falls withinthe scopes of the EU Network of Excellence MARBEF(Marine Biodiversity and Ecosystem Functioning).

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Documents

A taxonomic review of the genus Phaeocystis - AWIliar tubular extrusomes, a second non-colonial species from the north western Mediterranean Sea producing a lot of mucus, and a colonial