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Single Cell Analysis Reveals a New Microsporidia-Host Association in a Freshwater Lake

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Abstract

Microsporidia are a large group of obligate intracellular eukaryotic parasites. Recent studies suggest that their diversity can be huge in freshwater lake ecosystems especially in the < 150-µm size fraction. However, little is known about their hosts and therefore their impact on the trophic food web functioning. In this study, single cell analysis and fluorescence microscopy were used to detect new host-parasite association within rotifer communities in lake Aydat (France). Our analysis showed the existence of a potential new species belonging to the Crispospora genus able of infecting the rotifer Kellicottia with a high prevalence (42.5%) suggesting that Microsporidia could have a great impact on the rotifer populations’ regulation in lakes.

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Data Availability

All data and material are available in this publication and additional information online (supplementary material and supplementary figures). Sequences are available on GenBank, accession numbers from ON026091 to ON026096 for the microsporidian sequences and from ON033621 to ON033624 for the rotifers.

References

  1. Murareanu BM, Sukhdeo R, Qu R, Jiang J, Reinke AW (2021) Generation of a Microsporidia species attribute database and analysis of the extensive ecological and phenotypic diversity of Microsporidia. mBio 12:e01490-21. https://doi.org/10.1128/mBio.01490-21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Dubuffet A, Chauvet M, Moné A, Debroas D, Lepère C (2021) A phylogenetic framework to investigate the microsporidian communities through metabarcoding and its application to lake ecosystems. Environ Microbiol 23:4344–4359. https://doi.org/10.1111/1462-2920.15618

    Article  CAS  PubMed  Google Scholar 

  3. Chauvet M, Debroas D, Moné A, Dubuffet A, Lepère C (2022) Temporal variations of Microsporidia diversity and discovery of new host-parasite interactions in a lake ecosystem. Environ Microbiol. https://doi.org/10.1111/1462-2920.15950

    Article  PubMed  Google Scholar 

  4. Mikhailov KV, Simdyanov TG, Aleoshin VV (2016) Genomic survey of a hyperparasitic Microsporidian Amphiamblys sp. (Metchnikovellidae). Genome Biol Evol 9:454–467. https://doi.org/10.1093/gbe/evw235

    Article  CAS  PubMed Central  Google Scholar 

  5. Stentiford GD, Ramilo A, Abollo E, Kerr R, Bateman KS, Feist SW et al (2017) Hyperspora aquatica n.gn., n.sp. (Microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microspordian taxa. Parasitology 144:186–199. https://doi.org/10.1017/S0031182016001633

    Article  CAS  PubMed  Google Scholar 

  6. Fokin SI, Di Giuseppe G, Erra F, Dini F (2008) Euplotespora binucleata n. gen., n. sp. (Protozoa: Microsporidia), a parasite infecting the hypotrichous ciliate Euplotes woodruffi, with observations on microsporidian infections in ciliophora. J Eukaryot Microbiol 55:214–228. https://doi.org/10.1111/j.1550-7408.2008.00322.x

    Article  CAS  PubMed  Google Scholar 

  7. Yakovleva Y, Nassonova E, Lebedeva N, Lanzoni O, Petroni G, Potekhin A et al (2020) The first case of microsporidiosis in Paramecium. Parasitology 147:957–971. https://doi.org/10.1017/S0031182020000633

    Article  CAS  PubMed  Google Scholar 

  8. Gorbunov AK, Kosova AA (2001) Parasites in rotifers from the Volga delta. Hydrobiologia 446:51–55. https://doi.org/10.1023/A:1017569004998

    Article  Google Scholar 

  9. Wolska M, Mazurkiewicz-Zapalowicz K (2013) Parasites of zooplankton and periphyton assemblages in the littoral zone of lakes in Drawa National Park, Poland. Acta Mycol 48:51–59. https://doi.org/10.5586/am.2013.007

    Article  Google Scholar 

  10. Tokarev YS, Huang W-F, Solter LF, Malysh JM, Becnel JJ, Vossbrinck CR (2020) A formal redefinition of the genera Nosema and Vairimorpha (Microsporidia: Nosematidae) and reassignment of species based on molecular phylogenetics. J Invertebr Pathol 169:107279. https://doi.org/10.1016/j.jip.2019.107279

    Article  CAS  PubMed  Google Scholar 

  11. Tokarev YS, Voronin VN, Seliverstova EV, Pavlova OA, Issi IV (2010) Life cycle, ultrastructure, and molecular phylogeny of Crispospora chironomi g.n. sp.n. (Microsporidia: Terresporidia), a parasite of Chironomus plumosus L. (Diptera: Chironomidae). Parasitol Res 107:1381–1389. https://doi.org/10.1007/s00436-010-2012-x

    Article  PubMed  Google Scholar 

  12. Langdon PG, Ruiz Z, Brodersen KP, Foster IDL (2006) Assessing lake eutrophication using chironomids: understanding the nature of community response in different lake types. Freshw Biol 51:562–577. https://doi.org/10.1111/j.1365-2427.2005.01500.x

    Article  CAS  Google Scholar 

  13. Zhang Y, Xu S, Sun C, Dumont H, Han B-P (2021) A new set of highly efficient primers for COI amplification in rotifers. Mitochondrial DNA B 6:636–640. https://doi.org/10.1080/23802359.2021.1878951

    Article  Google Scholar 

  14. Zhang Y-N, Xu S-L, Huang Q, Liu P, Han B-P (2021) Application of COI primers 30F/885R in rotifers to regional species diversity in (sub)tropical China. Diversity 13:390. https://doi.org/10.3390/d13080390

    Article  Google Scholar 

  15. Barron GL, Szijarto E (1990) A new genus of the hyphomycetes endoparasitic in rotifers. Mycologia 82:134–137. https://doi.org/10.2307/3759974

    Article  Google Scholar 

  16. Thomas SH, Housley JM, Reynolds AN, Penczykowski RM, Kenline KH, Hardegree N et al (2011) The ecology and phylogeny of oomycete infections in Asplanchna rotifers: oomycete infections in Asplanchna. Freshw Biol 56:384–394. https://doi.org/10.1111/j.1365-2427.2010.02505.x

    Article  Google Scholar 

  17. Rico-Martínez R, Arzate-Ca rdenas MA, Robles D, Pérez-Legaspi I, Alvarado-Flores J, Santos Medrano GE (2016) Rotifers as models in toxicity screening of chemicals and environmental samples. In: Invertebrates – experimental models in toxicity screening. InTech, London, pp 57–99. https://doi.org/10.5772/61771

  18. Lair N, Oulad Ali H (1990) Grazing and assimilation rates of natural populations of planktonic rotifers Keratella cochlearis, Keratella quadrata and Kellicottia longispina in a eutrophic lake (Aydat, France). Hydrobiologia 194:119–131. https://doi.org/10.1007/BF00028413

    Article  Google Scholar 

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Acknowledgements

The authors are very grateful to Jonathan Colombet and Eugénie Carriere for their help with sampling. We also gratefully acknowledge the platform CLIC (CLermont-ferrand Imagerie Confocale, Université Clermont Auvergne) and especially Caroline Vachias for her assistance with the confocal microscopy. The work of MC and AM was supported by two PhD fellowships funded by the ‘Ministère de l’Enseignement Supérieur de la Recherche et de l’Innovation’.

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Correspondence to Cécile Lepère.

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Chauvet, M., Monjot, A., Moné, A. et al. Single Cell Analysis Reveals a New Microsporidia-Host Association in a Freshwater Lake. Microb Ecol 85, 1630–1633 (2023). https://doi.org/10.1007/s00248-022-02023-7

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