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Integrating Chytrid Fungal Parasites Into Plankton Ecology: Research Gaps and Needs

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Integrating Chytrid Fungal Parasites Into Plankton Ecology: Research Gaps and Needs Environmental Microbiology (2017) 19 (10), 3802–3822 doi:10.1111/1462-2920.13827 Minireview Integrating chytrid fungal parasites into plankton ecology: research gaps and needs Thijs Frenken, 1 Elisabet Alacid, 2 Stella A. Berger, 3 Elizabeth C. Bourne, 4,5 Melanie Gerphagnon, 5 Hans-Peter Grossart, 3,6 Alena S. Gsell, 1 Bas W. Ibelings, 7 Maiko Kagami, 8 Frithjof C. K upper,€ 9 Peter M. Letcher, 10 Adeline Loyau, 11,12,13 Takeshi Miki, 14,15 Jens C. Nejstgaard, 3 Serena Rasconi, 16 Albert Re n~e, 2 Thomas Rohrlack, 17 Keilor Rojas-Jimenez, 3,18 Dirk S. Schmeller, 12,13 Bettina Scholz, 19,20 Kensuke Seto, 8,21 Telesphore Sime-Ngando, 22 Assaf Sukenik, 23 Dedmer B. Van de Waal, 1 Silke Van den Wyngaert, 3 Ellen Van Donk, 1,24 Justyna Wolinska, 5,25 Christian Wurzbacher, 26,27 and Ramsy Agha 5* 1Department of Aquatic Ecology, Netherlands Institute of 12 Department of Conservation Biology, Helmholtz Center Ecology (NIOO-KNAW), Droevendaalsesteeg 10, for Environmental Research – UFZ, Permoserstrasse Wageningen, PB, 6708, The Netherlands. 15, Leipzig, 04318, Germany. 2Departament de Biologia Marina i Oceanografia, 13 ECOLAB, Universit e de Toulouse, CNRS, INPT, UPS, Institut de Cie`ncies del Mar (CSIC), Pg. Mar ıtim de la Toulouse, France. Barceloneta, 37-49, Barcelona, 08003, Spain. 14 Institute of Oceanography, National Taiwan University, 3Department of Experimental Limnology, Leibniz-Institute No.1 Section 4, Roosevelt Road, Taipei, 10617, Taiwan. of Freshwater Ecology and Inland Fisheries (IGB), Alte 15 Research Center for Environmental Changes, Fischerhuette 2, Stechlin, D-16775, Germany. Academia Sinica, No.128 Section 2, Academia Road, 4Berlin Center for Genomics in Biodiversity Research, Nankang, Taipei, 11529, Taiwan. 16 Konigin-Luise-Stra€ be 6-8, Berlin, D-14195, Germany. WasserCluster Lunz – Biological Station, Inter- 5Department of Ecosystem Research, Leibniz-Institute University Centre for Aquatic Ecosystem Research, of Freshwater Ecology and Inland Fisheries (IGB), A-3293 Lunz am See, Austria. 17 Muggelseedamm€ 301, Berlin, 12587, Germany. Faculty of Environmental Sciences and Natural 6Institute for Biochemistry and Biology, Potsdam Resource Management, Norwegian University of Life ˚ University, Maulbeerallee 2, Potsdam, D-14476, Germany. Sciences, P.O. Box 5003, NO-1432, A s, Norway. 18 7Department F.-A. Forel for Environmental and Aquatic Universidad Latina de Costa Rica, Campus San Sciences & Institute for Environmental Sciences, Pedro, Apdo, San Jose, 10138-1000, Costa Rica. 19 University of Geneva, 66 Boulevard Carl Vogt, Geneva BioPol ehf, Einb uastig 2, Skagastr ond€ 545, Iceland. 20 4, CH 1211, Switzerland. Faculty of Natural Resource Sciences, University of 8Department of Environmental Sciences, Faculty of Akureyri, Borgir v. Nordurslod, Akureyri, IS 600, Iceland. 21 Science, Toho University, 2-2-1, Miyama, Funabashi, Sugadaira Montane Research Center, University of Chiba, 274-8510, Japan. Tsukuba, 1278-294, Sugadaira-Kogen, Ueda, Nagano, 9Oceanlab, University of Aberdeen, Main Street, 386-2204, Japan. 22 Newburgh, Scotland, AB41 6AA, UK. Universit e Clermont Auvergne, UMR CNRS 6023 10 Department of Biological Sciences, The University of LMGE, Laboratoire Microorganismes: G enome et Alabama, 300 Hackberry Lane, Tuscaloosa, AL 35487, USA. Environnement (LMGE), Campus Universitaire des Cezeaux, Impasse Am elie Murat 1, CS 60026, Aubie`re, 11 Department of System Ecotoxicology, Helmholtz 63178, France. Center for Environmental Research – UFZ, 23 Kinneret Limnological Laboratory, Israel Permoserstrasse 15, 04318 Leipzig, Germany. Oceanographic & Limnological Research, P.O.Box 447, Migdal, 14950, Israel. Received 20 March, 2017; Revised: 9 June, 2017; accepted 10 24 June, 2017. *For correspondence. E-mail [email protected]; Department of Biology, University of Utrecht, Tel. 149 (30) 64 181 745; Fax 149 (30) 64 181 682. Padualaan 8, Utrecht, TB 3508, The Netherlands. VC 2017 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Research needs in plankton chytridiomycosis 3803 25 Institute of Biology, Freie Universit at€ Berlin, pharmaceuticals (Skja˚nes et al ., 2013). Parasite epidem- Konigin-Luise-Stra€ be 1-3, Berlin, 14195, Germany. ics can be especially devastating in such commercial 26 Department of Biological and Environmental Sciences, scale monocultures, posing severe monetary risk for the University of Gothenburg, Box 461, G oteborg,€ 405 30, algal industry (Carney and Lane, 2014). Sweden. Common parasites of phytoplankton include viruses, 27 Gothenburg Global Biodiversity Centre, Box 461, fungi, protists and pathogenic bacteria (Park et al ., 2004; Goteborg,€ SE-405 30, Sweden. Gachon et al ., 2010; Gerphagnon et al ., 2015). Among these, viruses raised the most interest in the previous decades (Bergh et al ., 1989) and their profound ecologi- cal implications were recognized soon after (Proctor and Fuhrman, 1990; Suttle et al ., 1990; Bratbak et al ., 1993; 1994; Fuhrman and Suttle, 1993; Fuhrman, 1999). In a Summary similar way, we perceive that scientific interest towards Chytridiomycota, often referred to as chytrids, can be fungal parasites of phytoplankton has gained momentum virulent parasites with the potential to inflict mass in recent years. This is in large part attributable to molec- mortalities on hosts, causing e.g. changes in ular environmental surveys revealing unexpected diversity phytoplankton size distributions and succession, of uncultured aquatic fungal organisms – i.e. the so- and the delay or suppression of bloom events. called Dark Matter Fungi (Grossart et al ., 2016) – which Molecular environmental surveys have revealed an is often dominated by members of the early diverging fun- unexpectedly large diversity of chytrids across a gal phylum Chytridiomycota (Monchy et al ., 2011; Jobard wide range of aquatic ecosystems worldwide. As a result, scientific interest towards fungal parasites of et al ., 2012; Lefe`vre et al ., 2012; Comeau et al ., 2016). phytoplankton has been gaining momentum in the Following initial work by Canter and Lund (Canter, 1946; past few years. Yet, we still know little about the Canter and Lund, 1948; 1951) and some later studies ecology of chytrids, their life cycles, phylogeny, host (Reynolds, 1973; Van Donk and Ringelberg, 1983), chy- specificity and range. Information on the contribution trids are raising renewed interest, as further evidence of chytrids to trophic interactions, as well as co- accumulates for their widespread distribution across cli- evolutionary feedbacks of fungal parasitism on host matic regions, in both marine and freshwater ecosystems populations is also limited. This paper synthesizes (Lefe`vre et al ., 2007; Lepe`re et al ., 2008; Wurzbacher ideas stressing the multifaceted biological relevance et al ., 2014; De Vargas et al ., 2015; Guti errez et al ., of phytoplankton chytridiomycosis, resulting from 2016; Hassett et al ., 2017; Hassett and Gradinger, 2016). discussions among an international team of chytrid Due to their inconspicuous morphological features, chy- researchers. It presents our view on the most pressing research needs for promoting the integration of trids have been often misidentified as bacterivorous flagel- chytrid fungi into aquatic ecology. lates and their role as parasites or saprobes in aquatic ecosystems have thus often been neglected. However, some chytrid taxa are lethal parasites (i.e. parasitoids) Introduction and have the potential to inflict mass mortalities on their hosts, causing changes in phytoplankton size distributions, Phytoplankton constitute the base of most aquatic food promotion of r-strategist hosts with fast turnover, delay or webs and play a pivotal role in biogeochemical cycles, suppression of bloom formation and successional accounting for more than half of the global carbon fixa- changes (Reynolds, 1973; Van Donk and Ringelberg, tion (Falkowski, 2012). Phytoplankton can be infected by 1983; Van Donk, 1989; Rasconi et al ., 2012; Gerphagnon a number of parasites, which have the potential to regu- et al ., 2015; Gleason et al ., 2015). Parasitism by chytrids late their abundance and dynamics and, thereby, modu- mediates inter- and intraspecific competition (Rohrlack late large scale ecological and/or biogeochemical et al ., 2015) and might promote diversity and polymor- processes. Parasitism constitutes an important evolu- phisms in host populations (Gsell et al ., 2013b). Chytrids tionary driver, which can promote genetic diversity in are characterized by a free-living motile stage in the form host populations and speciation (Hamilton, 1982; Wein- of single-flagellated zoospores that are assumed to bauer and Rassoulzadegan, 2004; Evison et al ., 2013). actively search for their hosts by chemotaxis (Canter and Parasites are involved in most trophic links within Jaworski, 1980; Muehlstein et al ., 1988). Upon settlement aquatic food webs, and can contribute significantly to on their host, chytrids penetrate the cell and develop rhi- the transfer of carbon and energy between trophic levels zoids to extract nutrients from it. Encysted zoospores (Amundsen et al ., 2009). Moreover, diverse phytoplank- develop into epibiotic sporangia which, once mature, ton taxa are also increasingly used in aquaculture indus- release new
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