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Current GeneticsMicroorganisms and Organelles ISSN 0172-8083Volume 61Number 3 Curr Genet (2015) 61:479-487DOI 10.1007/s00294-015-0501-2

The International Symposium on FungalStress: ISFUS

Drauzio E. N. Rangel, Alene Alder-Rangel, Ekaterina Dadachova, RogerD. Finlay, Jan Dijksterhuis, GilbertoU. L. Braga, et al.

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Curr Genet (2015) 61:479–487DOI 10.1007/s00294-015-0501-2

RESEARCH ARTICLE

The International Symposium on Fungal Stress: ISFUS

Drauzio E. N. Rangel · Alene Alder‑Rangel · Ekaterina Dadachova · Roger D. Finlay · Jan Dijksterhuis · Gilberto U. L. Braga · Luis M. Corrochano · John E. Hallsworth

Received: 1 June 2015 / Accepted: 3 June 2015 / Published online: 23 June 2015 © Springer-Verlag Berlin Heidelberg 2015

stress tolerance in other organisms. It is against this back-drop that a scientific meeting on fungal stress was held in São José dos Campos, Brazil, in October 2014. The meet-ing, hosted by Drauzio E. N. Rangel and Alene E. Alder-Rangel, and supported by the São Paulo Research Foun-dation (FAPESP), brought together more than 30 young, mid-career, and highly accomplished scientists from ten different countries. Here we summarize the highlights of the meeting.

Keywords Astrobiology · Biofuels · Compatible solutes · Entomopathogenic fungi · Erythritol and mannitol · Acid, alkali, chaotrope, ethanol, heat, hypoxic, osmotic, and salt stress · Saccharomyces cerevisiae · Trehalose · UV-B radiation tolerance

Abstract Fungi play central roles in many biological pro-cesses, influencing soil fertility, decomposition, cycling of minerals, and organic matter, plant health, and nutrition. They produce a wide spectrum of molecules, which are exploited in a range of industrial processes to manufacture foods, food preservatives, flavoring agents, and other useful biological products. Fungi can also be used as biological control agents of microbial pathogens, nematodes or insect pests, and affect plant growth, stress tolerance, and nutri-ent acquisition. Successful exploitation of fungi requires better understanding of the mechanisms that fungi use to cope with stress as well as the way in which they mediate

Communicated by D. E. N. Rangel.

This article is part ofthe Special Issue “Fungal Stress Responses”.

Electronic supplementary material The online version of this article (doi:10.1007/s00294-015-0501-2) contains supplementary material, which is available to authorized users.

D. E. N. Rangel (*) · A. Alder-Rangel Instituto de Pesquisa e Desenvolvimento, Universidade do Vale do Paraíba, São José dos Campos, SP 12244-000, Brazile-mail: drauzio@live.com

E. Dadachova Departments of Radiology and Microbiology and Immunology, Albert Einstein College of Medicine, 1695A Eastchester Road, Bronx, NY 10461, USA

R. D. Finlay Uppsala BioCenter, Department Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences, 75007 Uppsala, Sweden

J. Dijksterhuis CBS-KNAW Fungal Biodiversity Centre, Uppsalalaan 8, 3584, CT, Utrecht, The Netherlands

G. U. L. Braga Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP 14040-903, Brazil

L. M. Corrochano Departamento de Genética, Facultad de Biología, Universidad de Sevilla, Avenida Reina Mercedes 6, Apartado 1095, 41080 Seville, Spain

J. E. Hallsworth Institute for Global Food Security, School of Biological Sciences, Queen’s University Belfast, MBC, 97 Lisburn Road, Belfast BT9 7BL, UK

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Introduction

The solutions to many of the world’s current problems (e.g., food security, bioremediation of toxic chemicals in the envi-ronment, and the search for alternative sources of energy) will require further research on cellular and molecular biol-ogy, in particular the understanding of the mechanisms that fungi and yeasts use to cope with environmental stress. Due to their simplicity, fungi are also excellent models for study-ing the biology of eukaryotic cells and, in addition, are used for numerous applications within the various biotechnology industries. Understanding the fungal mechanisms of resist-ance to stress has important implications and consequences for fundamental as well as applied sciences. In agriculture, the interactions of plants and mycorrhizal fungi (Finlay 2008; Finlay et al. 2009), which improve phosphorus and nitrogen acquisition, should be better characterized and understood in order to increase global food production. Fur-thermore, the use of fungi as agents of biological control of insects (Rangel and Correia 2003; Alston et al. 2005; Faria and Wraight 2007; Li et al. 2010; Santi et al. 2010), nema-todes (Alston et al. 2005), plant-pathogenic fungi (Costa et al. 2013; Cray et al. 2015a), and mycoherbistats (Cli-quet et al. 2011) can reduce the use of chemical pesticides that endanger human health and the environment, without reducing crop yields. Moreover, saprotrophic activity of soil fungi, fungal plant pathogens, microbial pathogens of humans, food spoilage, and production of mycotoxins by fungi collectively impact global food security (Agrios 1997; Medina et al. 2014; Santos et al. 2015).

In industry, many useful compounds, such as antibiot-ics, enzymes, and other products, are produced by indus-trial strains of fungi including Penicillium or Aspergillus species (Singh and Pandey 2013). Trichoderma species are commonly used as a source of enzymes for cellulose degradation and also act as antagonists and mycoparasites of fungal plant pathogens (Druzhinina et al. 2011). Sac-charomyces cerevisiae is used for production of bioetha-nol as an alternative to fossil fuels (Zhao and Bai 2009; Cray et al. 2015b), thereby reducing the impact on climate change; fungi are used for the production of fermented foods (Schwan and Wheals 2004), drinks (Zhao and Bai 2009), and flavoring compounds (Hagedorn and Kapham-mer 1994), as well as for the bioremediation of polycyclic aromatic hydrocarbons, synthetic dyes, wood preservatives, synthetic polymers, pesticide residues, heavy metals, etc. (Pointing 2001; Gadd 2010). Fungi have evolved mecha-nisms to survive chemical and physical stresses, and these enable those species to drive biotechnological processes to generate the various stresses and stressors that can be imposed in industrial systems (Cray et al. 2015b). Further understanding of the mechanisms of coping with stress in these environments should help optimize process efficiency

in relation to biotechnological applications (Cray et al. 2015b).

In medicine, it is important to know how fungal patho-gens sense their environment to facilitate growth within otherwise healthy, or immunocompromised hosts. Studies on stress in fungi are at the forefront of recent advances and have important implications for human health, because the stress responses of human and animal pathogenic fungi are intrinsically linked to their virulence (Brown et al. 2007, 2014; Ene et al. 2014).

Thus, fungal stress response is a primary determinant of fungal ecology and has an enormous impact on human activities. Understanding fungal stress mechanisms and responses, and how to manipulate them to our advantage, are both important and urgent for agriculture, forestry, industry, and medicine. It is against this backdrop that the International Symposium on Fungal Stress-2014 was held.

The International Symposium on Fungal Stress

The International Symposium on Fungal Stress (ISFUS) (Fig. 1) that took place at the Universidade do Vale do Par-aíba in São José dos Campos, state of São Paulo, Brazil, during October 25–31, 2014 (web.univap.br/isfus) and was the first meeting of its kind to be organized around the topic of fungal stress.

The general objectives of the symposium were to (1) facilitate exploration of novel ideas and applications, and research collaborations, between diverse research groups whose work has relevance for fungal stress; (2) see solu-tions to enhance the stress tolerance of yeasts and fungi for agricultural, industrial and other applications; (3) share experiences, state-of-the-art research practices and details of local and international problems between Brazilian sci-entists and those from other countries; and (4) promote interest in, and awareness of, fungal stress biology.

The logo of the symposium (Fig. 1) represents one of the most-studied ascomycetes, Aspergillus nidulans, and illustrates some key stress parameters that fungi must cope to survive. These include ionizing radiation (Zhdanova et al. 2000; Dadachova and Casadevall 2008; Dighton et al. 2008), acidic and alkaline environments (Hallsworth and Magan 1996; St. Leger et al. 1998, 1999; Rangel 2011; Rangel et al. 2015b), hypoxic or anoxic stress (Hillmann et al. 2015; Rangel et al. 2015b), poisons and other types of chemicals that cause damage in fungi (Fernandes et al. 2010b; Rangel et al. 2008b, 2010a, 2011; Azevedo et al. 2014), solar UV radiation (Braga et al. 2001b, 2006; Fer-nandes et al. 2007), agricultural and industrial chaotropes, hydrophobes and other pollutants that fungi must be able to bioremediate (Pointing 2001; Hallsworth et al. 2003; Bhaganna et al. 2010; Gadd 2010; Ball and Hallsworth

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2015), osmotic stress (Solé et al. 2014; Hohmann 2015), nutritive stress or lack of carbon and nitrogen (Rangel et al. 2006, 2008b), and heat from solar irradiation and convec-tion (Rangel et al. 2005, 2010b; Fernandes et al. 2008; San-tos et al. 2011; Souza et al. 2014).

The ISFUS meeting aimed to both highlight recent research developments on fungal stress and foster collabo-ration among leaders and early-career scientists in the field. The conference was supported by a grant from FAPESP (São Paulo Research Foundation), and was organized by Drauzio E. N. Rangel and Alene Alder-Rangel with the help of Luis M. Corrochano and John E. Hallsworth; these four people formed the International Organizing Commit-tee. The Committee carefully selected a diversity of speak-ers in various stages of their careers that covered a wide spectrum of topics related to fungal stress. Conferences presentations included talks on sensory perception, sig-nal transduction, fungal biology in extreme environments, novel cellular stress mechanisms, and optimization of fun-gal metabolism or growth under conditions used by the bio-technology industry. In addition, the symposium included a tribute to two senior members of this research community,

Professors Anita D. Panek, from the Universidade Federal do Rio de Janeiro (Brazil), and Donald W. Roberts, from Utah State University (USA).

About 80 participants attended the ISFUS, including undergraduate and graduate students, postdocs, and faculty members, and the modest size of the meeting facilitated scientific interactions and the formation of friendships. The participants of the symposium (Figs. 2, 3) are experts in various disciplines, from fungal molecular biology and genetics to fungal physiology and pathogenesis. Many of the discussions were highly pertinent to Brazilian science as well as for the world economy: for example, the novel strategies to protect crop plants using entomopathogenic fungi for biological control of insects and new insights into yeast biology that can lead to improvements in efficiency or yields of biofuel fermentations. The proceedings and abstracts from the symposium are available online (web.univap.br/isfus as well in the Supplementary Material of this article), and a series of research articles and reviews highlighting the contributions to the conference were pub-lished in this Current Genetics special issue (Avalos and Limón 2014; Eleutherio et al. 2014; Fuller et al. 2014; Huarte-Bonnet et al. 2014; Lovett and St. Leger 2014; Medina et al. 2014; Ortiz-Urquiza and Keyhani 2014; Selbmann et al. 2014; Shalaby and Horwitz 2014; Solé et al. 2014; Alves et al. 2015; Braga et al. 2015; Fernandes et al. 2015; Hernández-Oñate and Herrera-Estrella 2015; Hillmann et al. 2015; Hohmann 2015; Rangel et al. 2015b).

Life‑Long Achievements Award to Anita D. Panek and Donald W. Roberts

Professor Anita Dolly Panek, born in Poland and settled in Brazil since 1930, was awarded a Life-Long Achieve-ment Award at ISFUS (Fig. 4) for 50 years work at the cutting edge of research on trehalose metabolism in yeast. Elis C. A. Eleutherio eloquently presented a biography of Anita D. Panek, which ended with a reading of the Rud-yard Kipling poem If. Panek has supervised 47 doctoral students, published 168 papers (cited almost 3000 times) and, at the age of 84, is still scientifically active. Her out-puts have given the international research community knowledge and understanding of fundamental aspects of trehalose metabolism and regulation, which provide an essential backdrop for understanding fungal stress biol-ogy, the biophysics of microbial systems and, indeed, the limits of life on Earth. It is no surprise, then, that early-, mid-, and late-stage microbiologists alike, who attended the ISFUS meeting, have cited the work of Panek through-out the course of their careers. Her work spans the physical chemistry of the trehalose molecule as a stress protectant, the biochemistry and genetics underlying various aspects of

Fig. 1 Logo of the International Symposium on Fungal Stress (ISFUS) that was hosted at the Universidade do Vale do Paraíba in São José dos Campos, SP, Brazil. ISFUS was supported by the São Paulo Research Foundation (FAPESP) and sponsored by the com-panies Lobov Científica, US BioSolutions, Biocontrol, Novozymes, Zeiss, and Altmann. This figure shows the possible stress conditions that fungi need to cope to survive such as ionizing radiation, acidic and alkaline environments, hypoxic or anoxic conditions, poisons in general such as genotoxic and oxidative products, UV radiation from Sun, pollution from industry and agriculture, salt stress, nutritive stress, and heat from solar radiation and other sources

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trehalose metabolism in S. cerevisiae, aspects of cell biol-ogy, and biotechnology. From 1959 to 1987, Panek devoted her studies to the regulation of trehalose metabolism in yeast cells (Panek 1959, 1962, 1963). Her group worked on the elucidation of the mechanism by which the hydro-lytic enzyme, Nth1, is activated, a mechanism that involves phosphorylation mediated by cyclic AMP-dependent pro-tein kinase (Ortiz et al. 1983) and in 1988 Panek was the first to establish a direct correlation between intracellular trehalose and cell resistance to freezing and dehydration (Coutinho et al. 1988). Since then, her group has dem-onstrated that this disaccharide is required for survival of diverse challenges, such as desiccation (Eleutherio et al. 1993a), heat (Eleutherio et al. 1993b), ethanol (Mansure et al. 1994), and oxidative stress (Herdeiro et al. 2006). Panek has received a number of accolades in recognition of her contributions to science: she is an Emeritus Professor of Universidade Federal do Rio de Janeiro, has achieved the top rating within the productivity sponsorship system from the National Research Council of Brazil (CNPq), member of the Brazilian Academy of Science, and is Com-mander of the Order of National Scientific Merit. Despite her achievements in the field of microbiology, Panek has

the heart of an artist; in fact, this may give rise her unwa-vering curiosity and creativity. In addition to her scholarly outputs, the ever-industrious Panek has also written and published books of other genre, including Carta aos Meus Netos (Letters to My Grandchildren). She has a coopera-tive and caring personality, and she has touched the lives of all those who have worked with her by her kind and grace-ful attitude to both life and work. The ISFUS-2014 meet-ing was honored by Anita D. Panek’s presence (Figs. 2, 3, 4), which added intellectual depth and provided a special ambience and warmth.

The work of Professor Donald W. Roberts (Fig. 5) was also recognized with a Life-Long Achievement Award at ISFUS, after 50+ years of leadership world-wide in the field of insect control using entomopathogenic fungi. A native of Phoenix, Arizona, USA, he received his PhD at the University of California, Berkeley in 1964, under Dr. Edward Steinhaus, working on toxins of Metarhizium anisopliae (Roberts 1966, 1969). While at Boyce Thomp-son Institute for Plant Research from 1965 to 1996, he was instrumental in making this institution an important center for insect pathology research. In addition to microbial con-trol of insects (Roberts et al. 1981; Roberts and St. Leger

Fig. 2 Speakers of the ISFUS, standing from left to right: Roger Finlay (Sweden), Jan Dijksterhuis (The Netherlands), Gilberto U.L. Braga (Brazil), Naresh Magan (UK), Nicolas Pedrini (Argentina), Francesc Posas (Spain), Pedro Moradas Ferreira (Portugal), Ekat-erina Dadachova (USA), Jennifer J. Loros (USA), Gertien Smits (The Netherlands), Jay C. Dunlap (USA), Kevin K. Fuller (USA), Karel van Laarhoven (The Netherlands), Nemat O. Keyhani (USA), Mirjam Bekker (The Netherlands), Brian R. Lovett (USA), Raymond J. St. Leger (USA), Márcia R. von Zeska Kress (Brazil), Stefan Hohmann

(Sweden), Everton K. K. Fernandes (Brazil), Patrícia Golo (Brazil), Donald W. Roberts in the computer after videoconference via Skype (USA). Seated: John E. Hallsworth (UK), Luis Corrochano (Spain), Anita D. Panek (Brazil), Drauzio E. N. Rangel (Brazil), Alene Alder-Rangel (USA/Brazil) and Alfredo Herrera-Estrella (Mexico). The speakers Enrique Cerdá-Olmedo (Spain), Elis C. A. Eleutherio (Brazil), Gustavo H. Goldman (Brazil), Javier Avalos (Spain), Johan Thevelein (Belgium), Olaf Kniemeyer (Germany), and Maria Célia Bertolini (Brazil) were also present but are not pictured here

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2004), his work with entomopathogenic fungi has included: fungal toxins (Roberts 1966, 1969; Kaijiang and Roberts 1986), fungal shelf life (Daoust and Roberts 1983a, b),

physiology of virulence (Daoust and Roberts 1982; St. Leger et al. 1991; Rangel et al. 2008a), molecular biology of fungi (St. Leger et al. 1996), and pathogens of medically important arthropods (Daoust and Roberts 1982), as well

Fig. 3 Speakers of the ISFUS, from left to right: Javier Avalos (Spain), Jennifer J. Loros in the front row (USA), [at the back] Ever-ton K. K. Fernandes (Brazil), Jay C. Dunlap (USA), Pedro Moradas Ferreira (Portugal), Enrique Cerdá-Olmedo (Spain), Jan Dijksterhuis (The Netherlands), Nicolas Pedrini (Argentina), [hidden at the back] Kevin K. Fuller (USA), Ekaterina Dadachova (USA), Mirjam Bekker (The Netherlands), Karel van Laarhoven (The Netherlands), Naresh Magan (UK), Nemat O. Keyhani (USA), [at the back] Roger Finlay (Sweden), Luis Corrochano (Spain), [at the back] Raymond J. St.

Leger (USA), Gustavo H. Goldman (Brazil), Brian Lovett (USA), [hidden at the back] Olaf Kniemeyer (Germany), Anita D. Panek (Brazil), Alfredo Herrera-Estrella (Mexico), [hidden at the back] Ger-tien Smits (The Netherlands), John E. Hallsworth (UK), Gilberto U. L. Braga (Brazil), [hidden in 2nd row] Elis C. A. Eleutherio (Brazil), Márcia Kress (Brazil), Francesc Posas (Spain), Alene Alder-Rangel (USA/Brazil), Stefan Hohmann (Sweden), Maria Célia Bertolini (Brazil), and Drauzio E. N. Rangel (Brazil). Johan Thevelein (Bel-gium) was also present but is not pictured here

Fig. 4 Professor Anita D. Panek receiving her Life-Long Achieve-ment Award at ISFUS-2014 from Drauzio E. N. Rangel (far left), Elis C. A. Eleutherio (center left), and Alene Alder-Rangel (far right)

Fig. 5 Professor Donald W. Roberts (left) after the PhD Commence-ment of Drauzio E. N. Rangel (right) at Utah State University (2006)

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as insect poxviruses (McCarthy et al. 1975). Roberts and his group have played a significant role in making Metarhi-zium an important model organism. When Metarhizium anisopliae was divided into several new species, one of these was named Metarhizium robertsii in his honor (Bis-choff et al. 2009). Roberts has always worked tenaciously to increase the use of insect-pathogenic fungi for biologi-cal control world-wide. His USAID Bean/Cowpea CRSP-funded project carried out in Brazil (1981–1992) made a major contribution to ensure the current position of Brazil as the world leading nation in research and use of fungal pathogens for insect biocontrol. Roberts has also conducted biocontrol projects in Nigeria, India, the Philippines, and United States, and more than 100 scholars from throughout the world have worked in his laboratory as students, post-doctoral fellows, and visiting scientists. He caringly pro-vides those working for him the freedom to explore their hypotheses and thereby experience the joys of scientific discovery, and to gain confidence from their own develop-ment (St. Leger 2010; Alder-Rangel 2015). After retiring from BTI, Roberts moved to Utah State University where he has continued to work, focusing on possible biocontrol agents for grasshoppers and the Mormon cricket (Roberts et al. 2007), improving tolerance of entomopathogenic fungi from UV radiation and heat (Braga et al. 2001a, c; Fernandes et al. 2009; Rangel et al. 2010b, 2012; Fernandes et al. 2011; Keyser et al. 2014), as well as methods for soil isolation of entomopathogenic fungi (Fernandes et al. 2010a, b; Rangel et al. 2010a). Roberts planned to give a presentation at the ISFUS on the implications of increased UV-B radiation on microbial control of insects but was prevented from traveling by a health problem. Thank-fully, he joined us via Skype, for the final presentation in which Raymond St. Leger spoke about Roberts’s life-long and continuing contributions to science, and then Patricia S. Golo presented the Roberts talk about UV-B radiation. All those who worked with Roberts were overjoyed with his involvement, and those who had not yet met him felt a sense of history to be joined by an academic giant of this field.

Footnote

The ISFUS-2014 produced a number of new collabora-tions: within a six-month period joint experiments have been set up, grant proposals submitted, and papers pub-lished from newly formed linkages (Alves et al. 2015; Cray et al. 2015b; Rangel et al. 2015a, b; Stevenson et al. 2015). Moreover, the meeting was cordial and stimulating, and the organizers are considering a series of international confer-ences on this topic.

Acknowledgments The Universidade do Vale do Paraíba in São José dos Campos, SP, Brazil hosted the International Symposium on Fungal Stress (ISFUS) in October 2014 organized by Drauzio E.N. Rangel, Alene Alder-Rangel, Luis M. Corrochano, and John E. Hallsworth with support from São Paulo Research Foundation (FAPESP). This Fungal Stress Responses special edition of Current Genetics was inspired by the International Symposium on Fungal Stress and invited by Stefan Hohmann, former Editor-in-Chief of Current Genetics. This work was supported by grants of the Brazil-ian National Council for Scientific and Technological Development (CNPq) 473104/2008-3, 478899/2010-6, PQ2 302312/2011-0, and PQ1D 308436/2014-8 for D.E.N.R. This review article was supported by a grant from São Paulo Research Foundation (FAPESP) of Bra-zil #2010/06374-1, 2013/50518-6 for D.E.N.R. and 2012/15204-8 for G.U.L.B. This review article was supported in part by a grant from FAPESP # 2014/01229-4. This work was also supported by European funds (European Regional Development Fund, ERDF), and the Span-ish Ministerio de Educación y Ciencia (BIO2012-38520) for L.M.C.

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