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Parasitoid chytridiomycete Ericiomyces syringoforeus gen. et sp. nov. has unique cellular structures to infect the host

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Abstract

Many fungi have been identified as pathogens of marine algae. Among them, Chytridiomycota have been revealed as relatively highly abundant, but much of the diversity known within these groups is almost entirely based on environmental sequencing data. Here, we present a novel chytridiomycete genus and species, characterized by light microscopical observations, ultrastructure, and molecular phylogenetic analysis of the parasitic chytrid of brackish-water dinoflagellate Kryptoperidinium foliaceum from the Baltic Sea. Phylogenetic analysis of rDNA sequences and the ultrastructure of the strain reveals that it represents a new family in the order Rhizophydiales. Ericiomyces syringoforeus gen. et sp. nov. is a parasitoid with a life cycle composed by zoospores, which attach to the host, encyst, and produce a rhizoidal system (haustorium). Unlike typical Rhizophydiales chytrids, sporangium develops as a lateral outgrowth of the encysted zoospore. The ultrastructural study revealed at least two unique traits: the syringe-like organelle in the cyst, which supposed to paralyze the host, and funnel-shaped structure anchoring sporangium in the host wall. Sporangium matures and produces new zoospores within 3 days. Multiple infections are common and then the life cycle is 1–2 days shorter compared to the duration when a single infection occurred. Cross-infection experiments showed that E. syringoforeus could only infect dinoflagellates, being K. foliaceum highly susceptible to infection by the chytrid parasitoid. The effects of some fungal epidemics on populations of Kryptoperidinium are discussed.

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Notes

  1. Restrictly speaking, most of the described marine chytrids occur, in fact, in brackish waters (0.5–30 psu) (e.g., Lepelletier et al. 2014b, Letcher et al. 2015). Below, we use “brackish” rather than “marine.”

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Acknowledgments

Light and electron microscopic studies and manuscript writing were supported by Russian Scientific Foundation grant 16-14-10302. SK and AV thank the Research Resource Centre for Molecular and Cell Technologies (RRC MCT) at St. Petersburg State University (SPbSU) for access to the EM facilities. EG, EA, and AR were supported by MINECO COPAS “Understanding top-down control in coastal bloom-forming protists” (CTM2017-86121-R). MK and KS were supported by JSPS KAKENHI grants 15KK0026 & 16H02943. AK and AP were supported by grant 251564 from Academy of Finland. The authors thank Dr. B.S.C. Leadbeater for English correction.

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Authors and Affiliations

  1. Zoological Institute of Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, Russia, 199034

    Sergey A. Karpov

  2. Department of Invertebrate Zoology, Biological Faculty, St. Petersburg State University, Universitetskaya nab. 7/9, St. Petersburg, Russia, 199034

    Sergey A. Karpov & Andrey E. Vishnyakov

  3. Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar (CSIC), Passeig Marítim de la Barceloneta 37-49, 08003, Barcelona, Catalonia, Spain

    Albert Reñé, Elisabet Alacid & Esther Garcés

  4. Graduate school of Environment and Information Sciences, Yokohama National University, Tokiwadai 79-7, Hodogayaku, Yokohama, Kanagawa, 240-8501, Japan

    Kensuke Seto & Maiko Kagami

  5. Department of Ecology and Evolutionary Biology, University of Michigan, 1105 North University, Ann Arbor, MI, 48109, USA

    Kensuke Seto

  6. Department of Zoology, University of Oxford, 11a Mansfield Rd, Oxford, OX1 3SZ, UK

    Elisabet Alacid

  7. Finnish Environment Institute, Marine Research Centre, Latokartanonkaari 11, 00790, Helsinki, Finland

    Aurora Paloheimo

  8. Department of Biological Oceanography, Leibniz Institute for Baltic Sea Research Warnemünde, Seestraße 15, 18119, Rostock, Germany

    Anke Kremp

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  1. Sergey A. Karpov
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  2. Albert Reñé
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  9. Esther Garcés
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Contributions

Anke Kremp, Esther Garcés, and Elisabet Alacid designed the study and Anke Kremp, Esther Garcés, Elisabet Alacid, and Aurora Paloheimo performed samplings. Elisabet Alacid and Aurora Paloheimo performed laboratory experiments. Sergey A. Karpov, Albert Reñé, and Andrey E. Vishnyakov performed LM and Albert Reñé performed SEM observations and culture sequencing. Albert Reñé and Kensuke Seto performed phylogenetic analyses. Sergey A. Karpov, Andrey E. Vishnyakov, Kensuke Seto, and Maiko Kagami performed TEM observations. Sergey A. Karpov and Albert Reñé conceptualized the manuscript. Sergey A. Karpov drafted the manuscript and all authors reviewed and edited it.

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Correspondence to Sergey A. Karpov.

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Supplementary Information

Supplementary Figure 1

Maximum likelihood phylogenetic tree of concatenated 18S + 5.8S + 28S rDNA sequences representing the diversity of Chytridiomycota. The sequence of Ericiomyces syringoforeus is in bold. Statistical support of the nodes is presented by the bootstrap value (%) and the Bayesian posterior probability. Only values >70% and > 0.95 respectively are shown. When only one of the values is below the threshold, it is indicated with a dashed line. (DOCX 26.0 kb)

Supplementary Figure 2

Maximum likelihood phylogenetic tree of 28S rDNA sequences representing the diversity of the Rhizophydiales. The sequence of Ericiomyces syringoforeus is in bold. Statistical support of the nodes is presented by the bootstrap value (%) and the Bayesian posterior probability. Only values >70% and > 0.95 respectively are shown. When only one of the values is below the threshold, it is indicated with a dashed line. (DOCX 35.7 kb)

Supplementary Figure 3

Maximum likelihood phylogenetic tree of 18S rDNA sequences representing the diversity of the Rhizophydiales. The sequence of Ericiomyces syringoforeus is in bold. Statistical support of the nodes is presented by the bootstrap value (%) and the Bayesian posterior probability. Only values >70% and > 0.95 respectively are shown. When only one of the values is below the threshold, it is indicated with a dashed line. (PDF 380 kb)

Supplementary Table S1

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Supplementary Table S2

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Karpov, S.A., Reñé, A., Vishnyakov, A.E. et al. Parasitoid chytridiomycete Ericiomyces syringoforeus gen. et sp. nov. has unique cellular structures to infect the host. Mycol Progress 20, 95–109 (2021). https://doi.org/10.1007/s11557-020-01652-x

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