Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-16T15:05:38.264Z Has data issue: false hasContentIssue false

Fitness and eco-physiological response of a chytrid fungal parasite infecting planktonic cyanobacteria to thermal and host genotype variation

Published online by Cambridge University Press:  26 February 2018

Ramsy Agha*
Affiliation:
Department of Ecosystem Research, Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 301, Berlin, 12587, Germany
Alina Gross
Affiliation:
Department of Ecosystem Research, Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 301, Berlin, 12587, Germany Institute of Biology, Freie Universität Berlin, Königin-Luise-Straße 1-3, Berlin, 14195, Germany
Melanie Gerphagnon
Affiliation:
Department of Ecosystem Research, Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 301, Berlin, 12587, Germany
Thomas Rohrlack
Affiliation:
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, NO-1432, Ås, Norway
Justyna Wolinska
Affiliation:
Department of Ecosystem Research, Leibniz-Institute of Freshwater Ecology and Inland Fisheries (IGB), Müggelseedamm 301, Berlin, 12587, Germany Institute of Biology, Freie Universität Berlin, Königin-Luise-Straße 1-3, Berlin, 14195, Germany
*
Author for correspondence: Ramsy Agha, E-mail: ramsyagha@gmail.com

Abstract

Understanding how individual parasite traits contribute to overall fitness, and how they are modulated by both external and host environment, is crucial for predicting disease outcome. Fungal (chytrid) parasites of phytoplankton are important yet poorly studied pathogens with the potential to modulate the abundance and composition of phytoplankton communities and to drive their evolution. Here, we studied life-history traits of a chytrid parasite infecting the planktonic, bloom-forming cyanobacterium Planktothrix spp. under host genotype and thermal variation. When expressing parasite fitness in terms of transmission success, disease outcome was largely modulated by temperature alone. Yet, a closer examination of individual parasite traits linked to different infection phases, such as (i) the establishment of the infection (i.e. intensity of infection) and (ii) the exploitation of host resources (i.e. size of reproductive structures and propagules), revealed differential host genotype and temperature × host genotype modulation, respectively. This illustrates how parasite fitness results from the interplay of individual parasite traits that are differentially controlled by host and external environment, and stresses the importance of combining multiple traits to gain insights into underlying infection mechanisms.

Type
Special Issue Research Article
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agha, R and Quesada, A (2014) Oligopeptides as biomarkers of cyanobacterial subpopulations. Toward an understanding of their biological role. Toxins 6, 19291950.Google Scholar
Agha, R, Saebelfeld, M, Manthey, C, Rohrlack, T and Wolinska, J (2016) Chytrid parasitism facilitates trophic transfer between bloom-forming cyanobacteria and zooplankton (Daphnia). Scientific Reports 6, 35039. doi: 10.1038/srep35039.Google Scholar
Antolin, MF (2008) Unpacking β: within-host dynamics and the evolutionary ecology of pathogen transmission. Annual Review of Ecology, Evolution, and Systematics 39, 415437.Google Scholar
Bates, D, Kliegl, R, Vasishth, S and Baayen, H (2015) Parsimonious mixed models. arXiv preprint arXiv:1506.04967.Google Scholar
Bates, DM (2010) lme4: Mixed-Effects Modeling with R. New York: Springer.Google Scholar
Braun, A (1856) Über Chytridium: eine Gattung einzelliger Schmarotzergewächse auf Algen und Infusorien. Printed in the printer of the Royal Academy of Sciences.Google Scholar
Bruning, K (1991 a) Effects of temperature and light on the population dynamics of the Asterionella-Rhizophydium association. Journal of Plankton Research 13, 707719.Google Scholar
Bruning, K (1991 b) Infection of the diatom Asterionella by a chytrid. I. Effects of light on reproduction and infectivity of the parasite. Journal of Plankton Research 13, 103117.Google Scholar
Bruning, K and Ringelberg, J (1987) The influence of phosphorus limitation of the diatom Asterionella formosa on the zoospore production of its fungal parasite Rhizophydium planktonicum. Aquatic Ecology 21, 4954.Google Scholar
Canter, HM (1947) Studies on British Chytrids: II. Some new monocentric chytrids. Transactions of the British Mycological Society 31, 94IN99105IN110.Google Scholar
Canter, HM and Jaworski, G (1979) The occurrence of a hypersensitive reaction in the planktonic diatom Asterionella formosa Hassall parasitized by the chytrid Rhizophydium planktonicum canter emend., in culture. New Phytologist 82, 187206.Google Scholar
Canter, HM and Jaworski, G (1981) The effect of light and darkness upon infection of Asterionella formosa Hassall by the chytrid Rhizophydium planktonicum canter emend. Annals of Botany 47, 1330.Google Scholar
Canter, HM and Lund, J (1948) Studies on plankton parasites. New Phytologist 47, 238261.Google Scholar
Canter, HM and Lund, J (1951) Fungal parasites of the phytoplankton. II: (studies on British chytrids. XII). Annals of Botany 129156.Google Scholar
De Bruin, A, Ibelings, BW, Kagami, M, Mooij, WM and Van Donk, E (2008) Adaptation of the fungal parasite Zygorhizidium planktonicum during 200 generations of growth on homogeneous and heterogeneous populations of its host, the diatom Asterionella formosa. Journal of Eukaryotic Microbiology 55, 6974.Google Scholar
Falkowski, P (2012) Ocean science: the power of plankton. Nature 483, S17S20.Google Scholar
Fels, D and Kaltz, O (2006) Temperature-dependent transmission and latency of Holospora undulata, a micronucleus-specific parasite of the ciliate Paramecium caudatum. Proceedings of the Royal Society of London B: Biological Sciences 273, 10311038.Google Scholar
Frenken, T, Alacid, E, Berger, SA, Bourne, EC, Gerphagnon, M, Grossart, HP, Gsell, AS, Ibelings, BW, Kagami, M and Agha, R (2017) Integrating chytrid fungal parasites into plankton ecology. Research gaps and needs. Environmental Microbiology 19, 38023822.Google Scholar
Futuyma, DJ (1986) Evolutionary Biology. Sunderland, Mass: Sinauer.Google Scholar
Gerphagnon, M, Latour, D, Colombet, J and Sime-Ngando, T (2013) A double staining method using SYTOX green and calcofluor white for studying fungal parasites of phytoplankton. Applied and Environmental Microbiology 79, 39433951.Google Scholar
Gerphagnon, M, Colombet, J, Latour, D and Sime-Ngando, T (2017) Spatial and temporal changes of parasitic chytrids of cyanobacteria. Scientific Reports 7, 6056. doi: 10.1038/s41598-017-06273-1.Google Scholar
Grossart, H-P, Wurzbacher, C, James, TY and Kagami, M (2016) Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi. Fungal Ecology 19, 2838.Google Scholar
Gsell, AS, de Senerpont Domis, LN, Van Donk, E and Ibelings, BW (2013 a) Temperature alters host genotype-specific susceptibility to chytrid infection. PLoS ONE 8, e71737.Google Scholar
Gsell, AS, de Senerpont Domis, LN, Verhoeven, KJ, Van Donk, E and Ibelings, BW (2013 b) Chytrid epidemics may increase genetic diversity of a diatom spring-bloom. The ISME Journal 7, 20572059.Google Scholar
Hassett, B and Gradinger, R (2016) Chytrids dominate Arctic marine fungal communities. Environmental Microbiology 18, 20012009.Google Scholar
Hinch, JM and Clarke, AE (1980) Adhesion of fungal zoospores to root surfaces is mediated by carbohydrate determinants of the root slime. Physiological Plant Pathology 16, 303IN301307IN302.Google Scholar
Ibelings, BW, De Bruin, A, Kagami, M, Rijkeboer, M, Brehm, M and Donk, EV (2004) Host parasite interactions between freshwater phytoplankton and chytrid fungi (chytridiomycota) 1. Journal of Phycology 40, 437453.Google Scholar
Kagami, M, von Elert, E, Ibelings, BW, de Bruin, A and Van Donk, E (2007) The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella. Proceedings of the Royal Society of London B: Biological Sciences 274, 15611566.Google Scholar
Kraaijeveld, AR and Godfray, HCJ (1999) Geographic patterns in the evolution of resistance and virulence in Drosophila and its parasitoids. The American Naturalist 153, S61S74.Google Scholar
Lefèvre, E, Roussel, B, Amblard, C and Sime-Ngando, T (2008) The molecular diversity of freshwater picoeukaryotes reveals high occurrence of putative parasitoids in the plankton. PLoS ONE 3, e2324.Google Scholar
Lepère, C, Domaizon, I and Debroas, D (2008) Unexpected importance of potential parasites in the composition of the freshwater small-eukaryote community. Applied and Environmental Microbiology 74, 29402949.Google Scholar
Lively, C (1999) Migration, virulence, and the geographic mosaic of adaptation by parasites. The American Naturalist 153, S34S47.Google Scholar
May, RM and Anderson, RM (1979) Population biology of infectious diseases: Part II. Nature 280, 455461.Google Scholar
May, RM and Anderson, Rt (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London B: Biological Sciences 219, 281313.Google Scholar
McCallum, H, Fenton, A, Hudson, PJ, Lee, B, Levick, B, Norman, R, Perkins, SE, Viney, M, Wilson, AJ and Lello, J (2017) Breaking beta: deconstructing the parasite transmission function. Philosophical Transactions of the Royal Society of London B: Biological Sciences 372, 20160084.Google Scholar
Mitchell, SE, Rogers, ES, Little, TJ and Read, AF (2005) Host-parasite and genotype-by-environment interactions: temperature modifies potential for selection by a sterilizing pathogen. Evolution 59, 7080.Google Scholar
Muehlstein, LK, Amon, JP and Leffler, DL (1988) Chemotaxis in the marine fungus Rhizophydium littoreum. Applied and Environmental Microbiology 54, 16681672.Google Scholar
Petre, B and Kamoun, S (2014) How do filamentous pathogens deliver effector proteins into plant cells? PLoS Biology 12, e1001801.Google Scholar
Rohrlack, T, Edvardsen, B, Skulberg, R, Halstvedt, CB, Utkilen, HC, Ptacnik, R and Skulberg, OM (2008) Oligopeptide chemotypes of the toxic freshwater cyanobacterium Planktothrix can form subpopulations with dissimilar ecological traits. Limnology and Oceanography 53, 1279.Google Scholar
Rohrlack, T, Christiansen, G and Kurmayer, R (2013) Putative antiparasite defensive system involving ribosomal and nonribosomal oligopeptides in cyanobacteria of the genus Planktothrix. Applied and Environmental Microbiology 79, 26422647.Google Scholar
Rohrlack, T, Haande, S, Molversmyr, Å and Kyle, M (2015) Environmental conditions determine the course and outcome of phytoplankton chytridiomycosis. PLoS ONE 10, e0145559.Google Scholar
Scholz, B, Küpper, FC, Vyverman, W, Ólafsson, HG and Karsten, U (2017) Chytridiomycosis of marine diatoms—The role of stress physiology and resistance in parasite-host recognition and accumulation of defense molecules. Marine Drugs 15, 26.Google Scholar
Sommer, U, Adrian, R, De Senerpont Domis, L, Elser, JJ, Gaedke, U, Ibelings, B, Jeppesen, E, Lürling, M, Molinero, JC and Mooij, WM (2012) Beyond the plankton ecology group (PEG) model: mechanisms driving plankton succession. Annual Review of Ecology, Evolution, and Systematics 43, 429448.Google Scholar
Sønstebø, JH and Rohrlack, T (2011) Possible implications of chytrid parasitism for population subdivision in freshwater cyanobacteria of the genus Planktothrix. Applied and Environmental Microbiology 77, 13441351.Google Scholar
Vale, P and Little, T (2009) Measuring parasite fitness under genetic and thermal variation. Heredity 103, 102.Google Scholar
Vale, P, Stjernman, M and Little, T (2008) Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions. Journal of Evolutionary Biology 21, 14181427.Google Scholar
Van den Wyngaert, S, Vanholsbeeck, O, Spaak, P and Ibelings, BW (2014) Parasite fitness traits under environmental variation: disentangling the roles of a chytrid's immediate host and external environment. Microbial Ecology 68, 645656.Google Scholar
Vredenburg, VT, Knapp, RA, Tunstall, TS and Briggs, CJ (2010) Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proceedings of the National Academy of Sciences 107, 96899694.Google Scholar
Welker, M and von Dohren, H (2006) Cyanobacterial peptides – Nature's own combinatorial biosynthesis. FEMS Microbiology Reviews 30, 530563.Google Scholar
Wolinska, J and King, KC (2009) Environment can alter selection in host–parasite interactions. Trends in Parasitology 25, 236244.Google Scholar