Taxonomic and Functional Dynamics During Chytrid Epidemics in an Aquatic Ecosystem

Overview

Journal Mol Ecol

Specialties Environmental Health
Molecular Biology

Date 2022 Aug 27

PMID 36028992

Authors

Luen-Luen Li

Pilar Delgado-Viscogliosi

Melanie Gerphagnon

Eric Viscogliosi

Urania Christaki

Telesphore Sime-Ngando

Sebastien Monchy

Affiliations

Soon will be listed here.

Abstract

Fungal parasitism is common in plankton communities and plays a crucial role in the ecosystem by balancing nutrient cycling in the food web. Previous studies of aquatic ecosystems revealed that zoosporic chytrid epidemics represent an important driving factor in phytoplankton seasonal successions. In this study, host-parasite dynamics in Lake Pavin (France) were investigated during the spring diatom bloom while following chytrid epidemics using next generation sequencing (NGS). Metabarcoding analyses were applied to study changes in the eukaryotic microbial community throughout diatom bloom-chytrid epidemics. Relative read abundances of metabarcoding data revealed potential "beneficiaries" and "victims" during the studied period. Subsequently, metatranscriptomic analyses on samples before and during the chytrid epidemic unveiled the active part of the community and functional/metabolic dynamics in association with the progress of chytrid infection. Diatom functions involving lipases, transporters, histones, vacuolar systems, the proteasome, proteases and DNA/RNA polymerases were more abundant during the diatom bloom. Chytrid functions related to a parasitic lifestyle including invasion, colonization and stress tolerance were up-regulated during the chytrid epidemic. In addition, functions related to the degradation/metabolism of proteins, lipids and chitin were in higher proportion in the community during the epidemic event. Results of NGS and bioinformatics analyses offered a panorama of dynamic biodiversity and biological functioning of the community.

Citing Articles

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PMID: 39915863 PMC: 11800578. DOI: 10.1186/s40168-024-02027-0.

Taxonomic and functional dynamics during chytrid epidemics in an aquatic ecosystem.

Li L, Delgado-Viscogliosi P, Gerphagnon M, Viscogliosi E, Christaki U, Sime-Ngando T Mol Ecol. 2022; 31(21):5618-5634.

PMID: 36028992 PMC: 9826485. DOI: 10.1111/mec.16675.

References

McKay R, Geider R, Laroche J . Physiological and Biochemical Response of the Photosynthetic Apparatus of Two Marine Diatoms to Fe Stress. Plant Physiol. 1997; 114(2):615-622. PMC: 158344. DOI: 10.1104/pp.114.2.615. View

Jajic I, Sarna T, Strzalka K . Senescence, Stress, and Reactive Oxygen Species. Plants (Basel). 2016; 4(3):393-411. PMC: 4844410. DOI: 10.3390/plants4030393. View

Jobard M, Rasconi S, Solinhac L, Cauchie H, Sime-Ngando T . Molecular and morphological diversity of fungi and the associated functions in three European nearby lakes. Environ Microbiol. 2012; 14(9):2480-94. DOI: 10.1111/j.1462-2920.2012.02771.x. View

Agha R, Saebelfeld M, Manthey C, Rohrlack T, Wolinska J . Chytrid parasitism facilitates trophic transfer between bloom-forming cyanobacteria and zooplankton (Daphnia). Sci Rep. 2016; 6:35039. PMC: 5062065. DOI: 10.1038/srep35039. View

Monchy S, Grattepanche J, Breton E, Meloni D, Sanciu G, Chabe M . Microplanktonic community structure in a coastal system relative to a Phaeocystis bloom inferred from morphological and tag pyrosequencing methods. PLoS One. 2012; 7(6):e39924. PMC: 3389043. DOI: 10.1371/journal.pone.0039924. View

Langmead B, Salzberg S . Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9(4):357-9. PMC: 3322381. DOI: 10.1038/nmeth.1923. View

Kagami M, Amano Y, Ishii N . Community structure of planktonic fungi and the impact of parasitic chytrids on phytoplankton in Lake Inba, Japan. Microb Ecol. 2011; 63(2):358-68. DOI: 10.1007/s00248-011-9913-9. View

Behnke A, Engel M, Christen R, Nebel M, Klein R, Stoeck T . Depicting more accurate pictures of protistan community complexity using pyrosequencing of hypervariable SSU rRNA gene regions. Environ Microbiol. 2011; 13(2):340-9. DOI: 10.1111/j.1462-2920.2010.02332.x. View

Kumar S, Stecher G, Tamura K . MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016; 33(7):1870-4. PMC: 8210823. DOI: 10.1093/molbev/msw054. View

10.

Guillou L, Bachar D, Audic S, Bass D, Berney C, Bittner L . The Protist Ribosomal Reference database (PR2): a catalog of unicellular eukaryote small sub-unit rRNA sequences with curated taxonomy. Nucleic Acids Res. 2012; 41(Database issue):D597-604. PMC: 3531120. DOI: 10.1093/nar/gks1160. View

11.

Anders S, Pyl P, Huber W . HTSeq--a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014; 31(2):166-9. PMC: 4287950. DOI: 10.1093/bioinformatics/btu638. View

12.

Rasconi S, Niquil N, Sime-Ngando T . Phytoplankton chytridiomycosis: community structure and infectivity of fungal parasites in aquatic ecosystems. Environ Microbiol. 2012; 14(8):2151-70. DOI: 10.1111/j.1462-2920.2011.02690.x. View

13.

Kozich J, Westcott S, Baxter N, Highlander S, Schloss P . Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013; 79(17):5112-20. PMC: 3753973. DOI: 10.1128/AEM.01043-13. View

14.

Kunin V, Engelbrektson A, Ochman H, Hugenholtz P . Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ Microbiol. 2009; 12(1):118-23. DOI: 10.1111/j.1462-2920.2009.02051.x. View

15.

Graff van Creveld S, Rosenwasser S, Schatz D, Koren I, Vardi A . Early perturbation in mitochondria redox homeostasis in response to environmental stress predicts cell fate in diatoms. ISME J. 2014; 9(2):385-95. PMC: 4303632. DOI: 10.1038/ismej.2014.136. View

16.

Salazar G, Paoli L, Alberti A, Huerta-Cepas J, Ruscheweyh H, Cuenca M . Gene Expression Changes and Community Turnover Differentially Shape the Global Ocean Metatranscriptome. Cell. 2019; 179(5):1068-1083.e21. PMC: 6912165. DOI: 10.1016/j.cell.2019.10.014. View

17.

Lopez-Garcia P, Philippe H, Gail F, Moreira D . Autochthonous eukaryotic diversity in hydrothermal sediment and experimental microcolonizers at the Mid-Atlantic Ridge. Proc Natl Acad Sci U S A. 2003; 100(2):697-702. PMC: 141059. DOI: 10.1073/pnas.0235779100. View

18.

Durkin C, Mock T, Armbrust E . Chitin in diatoms and its association with the cell wall. Eukaryot Cell. 2009; 8(7):1038-50. PMC: 2708456. DOI: 10.1128/EC.00079-09. View

19.

Lefevre E, Bardot C, Noel C, Carrias J, Viscogliosi E, Amblard C . Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environ Microbiol. 2007; 9(1):61-71. DOI: 10.1111/j.1462-2920.2006.01111.x. View

20.

Grabherr M, Haas B, Yassour M, Levin J, Thompson D, Amit I . Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011; 29(7):644-52. PMC: 3571712. DOI: 10.1038/nbt.1883. View