Single dominant diatom can host diverse parasitic fungi with different degree of host specificity

Recent molecular surveys revealed an unexpected diversity of mycoplankton in lakes and oceans. The early diverging fungal lineages are known to be prominent parasites of phytoplankton. However, due to missing fungal reference data, their identity and ecology remain mostly unknown. To overcome this p...

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Published in:Limnology and Oceanography
Main Authors: Kagami, Maiko, Seto, Kensuke, Nozaki, Daiki, Nakamura, Takaki, Wakana, Hirano, Wurzbacher, Christian
Format: Article in Journal/Newspaper
Language:unknown
Published: John Wiley & Sons, Inc. 2021
Subjects:
Online Access:https://hdl.handle.net/2027.42/167078
https://doi.org/10.1002/lno.11631
id ftumdeepblue:oai:deepblue.lib.umich.edu:2027.42/167078
record_format openpolar
institution Open Polar
collection University of Michigan: Deep Blue
op_collection_id ftumdeepblue
language unknown
topic Atmospheric and Oceanic Sciences
Science
spellingShingle Atmospheric and Oceanic Sciences
Science
Kagami, Maiko
Seto, Kensuke
Nozaki, Daiki
Nakamura, Takaki
Wakana, Hirano
Wurzbacher, Christian
Single dominant diatom can host diverse parasitic fungi with different degree of host specificity
topic_facet Atmospheric and Oceanic Sciences
Science
description Recent molecular surveys revealed an unexpected diversity of mycoplankton in lakes and oceans. The early diverging fungal lineages are known to be prominent parasites of phytoplankton. However, due to missing fungal reference data, their identity and ecology remain mostly unknown. To overcome this problem, we combined single‐spore‐based DNA barcoding during one sampling season of the eutrophic Lake Inba (Japan), which is dominated by two diatoms. By linking microscopically picked single fungal spore on two diatoms to subsequent DNA barcoding of ribosomal maker genes, we identified 12 distinct lineages, affiliated not only to the known parasitic phylum Chytridiomycota (chytrids), but also to the enigmatic phyla Rozellomycota and Aphelidiomycota. The detected Rozellomycota could be a hyperparasite of parasitic chytrid infecting diatoms. Host specificity appeared to be different among clades. However, the barcoding of single‐spore DNA could not clearly prove host specificity due to the limited number of samples and resolution in the targeted gene regions. The degree of host specificity was thus confirmed by the cross‐infection experiments. Five chytrid strains were generalists infecting all four diatoms strains, while the remaining three strains of chytrids were specialists exhibiting host preferences. Additional growth experiments indicated a trade‐off between host specificity and growth rate, so that generalists with more possible hosts grew slower than specialists with one host. Our results suggest that the combination of microscopy with single‐spore‐based barcoding is a promising approach to evaluate the complex host‐parasite interactions, while infection experiments can verify the interactions and shed light on the underlying ecological principles. Peer Reviewed http://deepblue.lib.umich.edu/bitstream/2027.42/167078/1/lno11631.pdf http://deepblue.lib.umich.edu/bitstream/2027.42/167078/2/lno11631_am.pdf http://deepblue.lib.umich.edu/bitstream/2027.42/167078/3/lno11631-sup-0002-FigureS1.pdf
format Article in Journal/Newspaper
author Kagami, Maiko
Seto, Kensuke
Nozaki, Daiki
Nakamura, Takaki
Wakana, Hirano
Wurzbacher, Christian
author_facet Kagami, Maiko
Seto, Kensuke
Nozaki, Daiki
Nakamura, Takaki
Wakana, Hirano
Wurzbacher, Christian
author_sort Kagami, Maiko
title Single dominant diatom can host diverse parasitic fungi with different degree of host specificity
title_short Single dominant diatom can host diverse parasitic fungi with different degree of host specificity
title_full Single dominant diatom can host diverse parasitic fungi with different degree of host specificity
title_fullStr Single dominant diatom can host diverse parasitic fungi with different degree of host specificity
title_full_unstemmed Single dominant diatom can host diverse parasitic fungi with different degree of host specificity
title_sort single dominant diatom can host diverse parasitic fungi with different degree of host specificity
publisher John Wiley & Sons, Inc.
publishDate 2021
url https://hdl.handle.net/2027.42/167078
https://doi.org/10.1002/lno.11631
genre Arctic
genre_facet Arctic
op_relation Kagami, Maiko; Seto, Kensuke; Nozaki, Daiki; Nakamura, Takaki; Wakana, Hirano; Wurzbacher, Christian (2021). "Single dominant diatom can host diverse parasitic fungi with different degree of host specificity." Limnology and Oceanography 66(3): 667-677.
0024-3590
1939-5590
https://hdl.handle.net/2027.42/167078
doi:10.1002/lno.11631
Limnology and Oceanography
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Maier, M. A., K. Uchii, T. D. Peterson, and M. Kagami. 2016. Evaluation of daphnid grazing on microscopic zoosporic fungi by using comparative threshold cycle quantitative PCR. Appl. Environ. Microbiol. 82: 3868 – 3874. doi:10.1128/AEM.00087-16
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Richards, T. A., and others. 2015. Molecular diversity and distribution of marine fungi across 130 European environmental samples. Proc. R. Soc. B Biol. Sci. 282: 20152243. doi:10.1098/rspb.2015.2243
Ronquist, F., and others. 2012. MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539 – 542. doi:10.1093/sysbio/sys029
Schmid‐Hempel, P. 2008. Parasite immune evasion: A momentous molecular war. Trends Ecol. Evol. 23: 318 – 326. doi:10.1016/j.tree.2008.02.011
Seto, K., M. Kagami, and Y. Degawa. 2017. Phylogenetic position of parasitic chytrids on diatoms: Characterization of a novel clade in chytridiomycota. J. Eukaryot. Microbiol. 64: 383 – 393. doi:10.1111/jeu.12373
Seto, K., and Y. Degawa. 2018. Pendulichytrium sphaericum gen. et sp. nov. (Chytridiales, Chytriomycetaceae), a new chytrid parasitic on the diatom, Aulacoseira granulata. Mycoscience 59: 59 – 66. doi:10.1016/j.myc.2017.08.004
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Van den Wyngaert, S., K. Rojas‐Jimenez, K. Seto, M. Kagami, and H.‐P. Grossart. 2018. Diversity and hidden host specificity of chytrids infecting colonial volvocacean algae. J. Eukaryot. Microbiol. 65: 870 – 881. doi:10.1111/jeu.12632
van Donk, E., and J. Ringelberg. 1983. The effect of fungal parasitism on the succession of diatoms in Lake Maarsseveen I (The Netherlands). Freshw. Biol. 13: 241 – 251. doi:10.1111/j.1365-2427.1983.tb00674.x
Wurzbacher, C., E. Larsson, J. Bengtsson‐Palme, S. Van den Wyngaert, S. Svantesson, E. Kristiansson, M. Kagami, and R. H. Nilsson. 2019. Introducing ribosomal tandem repeat barcoding for fungi. Mol. Ecol. Resour. 19: 118 – 127. doi:10.1111/1755-0998.12944
Alacid, E., M. G. Park, M. Turon, K. Petrou, and E. Garcés. 2016. A game of Russian roulette for a generalist dinoflagellate parasitoid: Host susceptibility is the key to success. Front. Microbiol. 7: 1 – 13. doi:10.3389/fmicb.2016.00769
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Canter, H. M., and G. H. M. Jaworski. 1978. The Isolation, Maintenance and Host Range Studies of a Chytrid Rhizophydium planktonicum Canter emend., Parasitic on Asterionella formosa Hassall. Annals of Botany 42 ( 4 ): 967 – 979. doi:10.1093/oxfordjournals.aob.a085536.
Canter, H. M., and G. H. M. Jaworski. 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 Phytol. 82: 187 – 206. doi:10.1111/j.1469-8137.1979.tb07574.x
Capella‐Gutiérrez, S., J. M. Silla‐Martínez, and T. Gabaldón. 2009. trimAl: A tool for automated alignment trimming in large‐scale phylogenetic analyses. Bioinformatics 25: 1972 – 1973. doi:10.1093/bioinformatics/btp348
Comeau, A. M., W. F. Vincent, L. Bernier, and C. Lovejoy. 2016. Novel chytrid lineages dominate fungal sequences in diverse marine and freshwater habitats. Sci. Rep. 6: 30120. doi:10.1038/srep30120
Corsaro, D., J. Walochnik, D. Venditti, B. Hauröder, and R. Michel. 2020. Solving an old enigma: Morellospora saccamoebae gen. nov., sp. nov. (Rozellomycota), a Sphaerita‐like parasite of free‐living amoebae. Parasitol. Res. 119: 925 – 934. doi:10.1007/s00436-020-06623-5
De Bruin, A., B. W. Ibelings, M. Rijkeboer, M. Brehm, and E. Van Donk. 2004. Genetic variation in Asterionella formosa (Bacillariophyceae): Is it linked to frequent epidemics of host‐specific parasitic fungi? J. Phycol. 40: 823 – 830. doi:10.1111/j.1529-8817.2004.04006.x
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Grossart, H. P., S. Van den Wyngaert, M. Kagami, C. Wurzbacher, M. Cunliffe, and K. Rojas‐Jimenez. 2019. Fungi in aquatic ecosystems. Nat. Rev. Microbiol. 17: 339 – 354. doi:10.1038/s41579-019-0175-8
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spelling ftumdeepblue:oai:deepblue.lib.umich.edu:2027.42/167078 2023-08-20T04:03:12+02:00 Single dominant diatom can host diverse parasitic fungi with different degree of host specificity Kagami, Maiko Seto, Kensuke Nozaki, Daiki Nakamura, Takaki Wakana, Hirano Wurzbacher, Christian 2021-03 application/pdf https://hdl.handle.net/2027.42/167078 https://doi.org/10.1002/lno.11631 unknown John Wiley & Sons, Inc. Kagami, Maiko; Seto, Kensuke; Nozaki, Daiki; Nakamura, Takaki; Wakana, Hirano; Wurzbacher, Christian (2021). "Single dominant diatom can host diverse parasitic fungi with different degree of host specificity." Limnology and Oceanography 66(3): 667-677. 0024-3590 1939-5590 https://hdl.handle.net/2027.42/167078 doi:10.1002/lno.11631 Limnology and Oceanography Rojas‐Jimenez, K., C. Wurzbacher, E. C. Bourne, A. Chiuchiolo, J. C. Priscu, and H. P. Grossart. 2017. Early diverging lineages within Cryptomycota and Chytridiomycota dominate the fungal communities in ice‐covered lakes of the McMurdo Dry Valleys, Antarctica. Sci. Rep. 7: 1 – 11. doi:10.1038/s41598-017-15598-w Maier, M. A., K. Uchii, T. D. Peterson, and M. Kagami. 2016. Evaluation of daphnid grazing on microscopic zoosporic fungi by using comparative threshold cycle quantitative PCR. Appl. Environ. Microbiol. 82: 3868 – 3874. doi:10.1128/AEM.00087-16 Mills, C. G., R. J. Allen, and R. A. Blythe. 2020. Resource spectrum engineering by specialist species can shift the specialist‐generalist balance. Theor. Ecol. 13: 149 – 163. doi:10.1007/s12080-019-00436-8 Poulin, R., and D. B. Keeney. 2008. Host specificity under molecular and experimental scrutiny. Trends Parasitol. 24: 24 – 28. doi:10.1016/j.pt.2007.10.002 Poulin, R., B. R. Krasnov, and D. Mouillot. 2011. Host specificity in phylogenetic and geographic space. Trends Parasitol. 27: 355 – 361. doi:10.1016/j.pt.2011.05.003 Rasconi, S., M. Jobard, L. Jouve, and T. Sime‐Ngando. 2009. Use of calcofluor white for detection, identification, and quantification of phytoplanktonic fungal parasites. Appl. Environ. Microbiol. 75: 2545 – 2553. doi:10.1128/AEM.02211-08 Richards, T. A., and others. 2015. Molecular diversity and distribution of marine fungi across 130 European environmental samples. Proc. R. Soc. B Biol. Sci. 282: 20152243. doi:10.1098/rspb.2015.2243 Ronquist, F., and others. 2012. MrBayes 3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539 – 542. doi:10.1093/sysbio/sys029 Schmid‐Hempel, P. 2008. Parasite immune evasion: A momentous molecular war. Trends Ecol. Evol. 23: 318 – 326. doi:10.1016/j.tree.2008.02.011 Seto, K., M. Kagami, and Y. Degawa. 2017. Phylogenetic position of parasitic chytrids on diatoms: Characterization of a novel clade in chytridiomycota. J. Eukaryot. Microbiol. 64: 383 – 393. doi:10.1111/jeu.12373 Seto, K., and Y. Degawa. 2018. Pendulichytrium sphaericum gen. et sp. nov. (Chytridiales, Chytriomycetaceae), a new chytrid parasitic on the diatom, Aulacoseira granulata. Mycoscience 59: 59 – 66. doi:10.1016/j.myc.2017.08.004 Seto, K., S. Van Den Wyngaert, Y. Degawa, and M. Kagami. 2020. Taxonomic revision of the genus Zygorhizidium: Zygorhizidiales and Zygophlyctidales ord. nov. (Chytridiomycetes, Chytridiomycota). Fungal Syst. Evol. 5: 17 – 38. doi:10.3114/fuse.2020.05.02 Stamatakis, A. 2014. RAxML version 8: A tool for phylogenetic analysis and post‐analysis of large phylogenies. Bioinformatics 30: 1312 – 1313. doi:10.1093/bioinformatics/btu033 Stein, J. R. 1973. In J. R. Stein. [ed.], Handbook of phycological methods: Culture methods and growth measurements (p. 460). Cambridge University Press. Taylor, J. D., and M. Cunliffe. 2016. Multi‐year assessment of coastal planktonic fungi reveals environmental drivers of diversity and abundance. ISME J. 10: 2118 – 2128. doi:10.1038/ismej.2016.24 Tedersoo, L., M. Bahram, R. Puusepp, R. H. Nilsson, and T. Y. James. 2017. Novel soil‐inhabiting clades fill gaps in the fungal tree of life. Microbiome 5: 1 – 10. doi:10.1186/s40168-017-0259-5 Truett, G. E., P. Heeger, R. L. Mynatt, A. A. Truett, J. A. Walker, and M. L. Warman. 2000. Preparation of PCR‐quality mouse genomic DNA with hot sodium hydroxide and tris (HotSHOT). Biotechniques 29: 52 – 54. doi:10.1016/j.jacc.2014.05.073 Van den Wyngaert, S., K. Rojas‐Jimenez, K. Seto, M. Kagami, and H.‐P. Grossart. 2018. Diversity and hidden host specificity of chytrids infecting colonial volvocacean algae. J. Eukaryot. Microbiol. 65: 870 – 881. doi:10.1111/jeu.12632 van Donk, E., and J. Ringelberg. 1983. The effect of fungal parasitism on the succession of diatoms in Lake Maarsseveen I (The Netherlands). Freshw. Biol. 13: 241 – 251. doi:10.1111/j.1365-2427.1983.tb00674.x Wurzbacher, C., E. Larsson, J. Bengtsson‐Palme, S. Van den Wyngaert, S. Svantesson, E. Kristiansson, M. Kagami, and R. H. Nilsson. 2019. Introducing ribosomal tandem repeat barcoding for fungi. Mol. Ecol. Resour. 19: 118 – 127. doi:10.1111/1755-0998.12944 Alacid, E., M. G. Park, M. Turon, K. Petrou, and E. Garcés. 2016. A game of Russian roulette for a generalist dinoflagellate parasitoid: Host susceptibility is the key to success. Front. Microbiol. 7: 1 – 13. doi:10.3389/fmicb.2016.00769 Amend, A., and others. 2019. Fungi in the marine environment: Open questions and unsolved problems. mBio 10: 1 – 15. doi:10.1128/mBio.01189-18 Canter, H. M. 1969. Studies on British Chytrids. XXIX. A taxonomic revision of certain fungi found on the diatom Asterionella. Bot. J. Linn. Soc. 62: 267 – 278. doi:10.1111/j.1095-8339.1969.tb01970.x Canter, H. M., and G. H. M. Jaworski. 1978. The Isolation, Maintenance and Host Range Studies of a Chytrid Rhizophydium planktonicum Canter emend., Parasitic on Asterionella formosa Hassall. Annals of Botany 42 ( 4 ): 967 – 979. doi:10.1093/oxfordjournals.aob.a085536. Canter, H. M., and G. H. M. Jaworski. 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 Phytol. 82: 187 – 206. doi:10.1111/j.1469-8137.1979.tb07574.x Capella‐Gutiérrez, S., J. M. Silla‐Martínez, and T. Gabaldón. 2009. trimAl: A tool for automated alignment trimming in large‐scale phylogenetic analyses. Bioinformatics 25: 1972 – 1973. doi:10.1093/bioinformatics/btp348 Comeau, A. M., W. F. Vincent, L. Bernier, and C. Lovejoy. 2016. Novel chytrid lineages dominate fungal sequences in diverse marine and freshwater habitats. Sci. Rep. 6: 30120. doi:10.1038/srep30120 Corsaro, D., J. Walochnik, D. Venditti, B. Hauröder, and R. Michel. 2020. Solving an old enigma: Morellospora saccamoebae gen. nov., sp. nov. (Rozellomycota), a Sphaerita‐like parasite of free‐living amoebae. Parasitol. Res. 119: 925 – 934. doi:10.1007/s00436-020-06623-5 De Bruin, A., B. W. Ibelings, M. Rijkeboer, M. Brehm, and E. Van Donk. 2004. Genetic variation in Asterionella formosa (Bacillariophyceae): Is it linked to frequent epidemics of host‐specific parasitic fungi? J. Phycol. 40: 823 – 830. doi:10.1111/j.1529-8817.2004.04006.x Frenken, T., and others. 2017. Integrating chytrid fungal parasites into plankton ecology: Research gaps and needs. Environ. Microbiol. 19: 3802 – 3822. doi:10.1111/1462-2920.13827 Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19: 207 – 233. doi:10.1146/annurev.es.19.110188.001231 Gromov, B. V., A. V. Plujusch, and K. A. Mamkaeva. 1999. Morphology and possible host range of Rhizophydium algavorum sp. nov. (Chytridiales) ‐ an obligate parasite of algae. Protist 1: 62 – 65. doi:10.1093/nar/gkm911 Grossart, H. P., C. Wurzbacher, T. Y. James, and M. Kagami. 2016. Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi. Fungal Ecol. 19: 28 – 38. doi:10.1016/j.funeco.2015.06.004 Grossart, H. P., S. Van den Wyngaert, M. Kagami, C. Wurzbacher, M. Cunliffe, and K. Rojas‐Jimenez. 2019. Fungi in aquatic ecosystems. Nat. Rev. Microbiol. 17: 339 – 354. doi:10.1038/s41579-019-0175-8 Gsell, A. S., L. N. de Senerpont Domis, E. van Donk, and B. W. Ibelings. 2013. Temperature alters host genotype‐specific susceptibility to chytrid infection. PLoS One 8: e71737. doi:10.1371/journal.pone.0071737 Gutman, J., A. Zarka, and S. Boussiba. 2009. The host‐range of Paraphysoderma sedebokerensis, a chytrid that infects Haematococcus pluvialis. Eur. J. Phycol. 44: 509 – 514. doi:10.1080/09670260903161024 Haag, K. L., T. Y. James, J.‐F. Pombert, R. Larsson, T. M. M. Schaer, D. Refardt, and D. 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Ecol. 63: 358 – 368. doi:10.1007/s00248-011-9913-9 IndexNoFollow Atmospheric and Oceanic Sciences Science Article 2021 ftumdeepblue https://doi.org/10.1002/lno.1163110.1038/s41598-017-15598-w10.1128/AEM.00087-1610.1007/s12080-019-00436-810.1016/j.pt.2007.10.00210.1016/j.pt.2011.05.00310.1128/AEM.02211-0810.1098/rspb.2015.224310.1093/sysbio/sys02910.1016/j.tree.2008.02.01110.1111/jeu.1 2023-07-31T20:28:12Z Recent molecular surveys revealed an unexpected diversity of mycoplankton in lakes and oceans. The early diverging fungal lineages are known to be prominent parasites of phytoplankton. However, due to missing fungal reference data, their identity and ecology remain mostly unknown. To overcome this problem, we combined single‐spore‐based DNA barcoding during one sampling season of the eutrophic Lake Inba (Japan), which is dominated by two diatoms. By linking microscopically picked single fungal spore on two diatoms to subsequent DNA barcoding of ribosomal maker genes, we identified 12 distinct lineages, affiliated not only to the known parasitic phylum Chytridiomycota (chytrids), but also to the enigmatic phyla Rozellomycota and Aphelidiomycota. The detected Rozellomycota could be a hyperparasite of parasitic chytrid infecting diatoms. Host specificity appeared to be different among clades. However, the barcoding of single‐spore DNA could not clearly prove host specificity due to the limited number of samples and resolution in the targeted gene regions. The degree of host specificity was thus confirmed by the cross‐infection experiments. Five chytrid strains were generalists infecting all four diatoms strains, while the remaining three strains of chytrids were specialists exhibiting host preferences. Additional growth experiments indicated a trade‐off between host specificity and growth rate, so that generalists with more possible hosts grew slower than specialists with one host. Our results suggest that the combination of microscopy with single‐spore‐based barcoding is a promising approach to evaluate the complex host‐parasite interactions, while infection experiments can verify the interactions and shed light on the underlying ecological principles. Peer Reviewed http://deepblue.lib.umich.edu/bitstream/2027.42/167078/1/lno11631.pdf http://deepblue.lib.umich.edu/bitstream/2027.42/167078/2/lno11631_am.pdf http://deepblue.lib.umich.edu/bitstream/2027.42/167078/3/lno11631-sup-0002-FigureS1.pdf Article in Journal/Newspaper Arctic University of Michigan: Deep Blue Limnology and Oceanography 66 3 667 677