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.
Similar content being viewed by others
References
Alacid E, Reñé A, Gallisai R, Paloheimo A, Garcés E, Kremp A (in press) Description of two new coexisting parasitoids of blooming dinoflagellates in the Baltic Sea: Parvilucifera catillosa sp. nov. and Parvilucifera sp. (Perkinsea, Alveolata). Harmful algae
Alster A, Zohary T (2007) Interactions between the bloom-forming dinoflagellate Peridinium gatunense and the chytrid fungus Phlyctochytrium sp. Hidrobiologia 578:131–139
Amend A, Burgaud G, Cunliffe M, Edgcomb VP, Ettinger CL, Gutiérrez MH, Heitman J, Hom EFY, Ianiri G, Jones AC, Kagami M, Picard KT, Quandt CA, Raghukumar S, Riquelme M, Stajich J, Vargas-Muñiz J, Walker AK, Yarden O, Gladfelter AS (2019) Fungi in the marine environment: open questions and unsolved problems. mBio 10:e01189–18. https://doi.org/10.1128/mBio.01189-18
Beakes GW, Canter HM, Jaworski GHM (1993) Sporangium differentiation and zoospore fine-structure of the chytrid Rhizophydium planktonicum, a fungal parasite of Asterionella formosa. Mycol Res 97:1059–1074
Canter HM (1968) Studies on British chytrids. XXVIII. Rhizophydinium nobile sp. nov., parasitic on the resting spore of Ceratium hirundinella O.F.Müll. From the plankton. Proc Linn Soc Lond 179:197–201
Canter HN, Heaney SI (1984) Observations on zoosporic fungi of Ceratium spp. in lakes of the English Lake District; importance for phytoplankton population dynamics. New Phytol 97:601–612
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973
Comeau AM (2016) Novel chytrid lineages dominate fungal sequences in diverse marine and freshwater habitats. Sci Rep 6:30120
Couch JN (1938) A new species of Chytridium from mountain Lake, Virginia. Jour Elisha Mitchell Sci Soc 64:256–259
Kremp A, Lindholm T, Dressler N, Erler K, Gerdts G, Eirtovaara S, Leskinen E (2009) Bloom forming Alexandrium ostenfeldii (Dinophyceae) in shallow waters of the Åland Archipelago, Northern Baltic Sea. Harmful Algae 8:318–328
Dangeard P-A (1888) Recherches sur les algues inférieures. Annales des Sciences Naturelles Botanique 7:105–175
Frenken T, Alacid E, Berger S, Bourne EC, Gerphagnon M, Grossart H-P, Gsell AS, Ibelings BW, Kagami M, Kupper FC, Letcher PM, Loyau A, Miki T, Nejstgaard JC, Rasconi S, Reñé A, Rohrlack T, Rojas-Jimenez K, Schmeller D, Scholz B, Seto K, Sime-Ngando T, Sukenik A, Van de Waal DB, Van den Wyngaert S, Van Donk E, Wolinska J, Wurzbacher C, Agha R (2017) Integrating chytrid fungal parasites into plankton ecology. Research gaps and needs. Environ Microbiol 19:3802–3822
Garvetto A, Badis Y, Perrineau MM, Rad-Menéndez C, Bresnan E, Gachon CM (2019) Chytrid infecting the bloom-forming marine diatom Skeletonema sp.: morphology, phylogeny and distribution of a novel species within the Rhizophydiales. Fungal biology 123:471–480
Gleason FH, Jephcott TG, Küpper FC, Gerphagnon M, Sime-Ngando T, Karpov S, Guillou L, Van Ogtrop FF (2015) Potential roles for recently discovered chytrid parasites in the dynamics of harmful algal blooms. Fungal Biology Reviews 29:20–33
Golubeva OG (1995) Keys to mushrooms of Russia. Class Chytridiomycetes. Issue 1. SPb, "World and Family-95" (in Russian)
Hakanen P, Suikkanen S, Franzén J, Franzén H, Kankaanpää H, Kremp A (2012) Bloom and toxin dynamics of Alexandrium ostenfeldii in a shallow embayment at the SW coast of Finland, northern Baltic Sea. Harmful Algae 15:91–99
Hansen G, Daugbjerg N, Henriksen P (2000) Comparative study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. Nov. (=Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. J Phycol 36:394–410
Jones EBG, Suetrong S, Sakayaroj J, Bahkali A, Abdel-Wahab M, Boekhout T, Pang K-L (2015) Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers 73:1–72
Jones EBG, Pang K, Abdel-Wahab MA et al (2019) An online resource for marine fungi. Fungal Divers 96:347–433. https://doi.org/10.1007/s13225-019-00426-5
Kagami M, de Bruin A, Ibelings BW, Van Donk E (2007) Parasitic chytrids: their effects on phytoplankton communities and food-web dynamics. Hydrobiologia 578:113–129
Karling JS (1938) Two new operculate chytrids. Mycologia 30:302–312
Karpov SA, Lopez-Garcıa P, Mamkaeva MA, Tcvetkova VS, Vishnyakov AE, Klimov VI, Moreira D (2018) The chytrid-like parasites of algae Amoeboradix gromovi gen. et sp. nov. and Sanchytrium tribonematis belong to a new fungal lineage. Protist 169:122–140
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166
Koch WJ (1951) Studies of the Chytridium, with observations on the sexually reproducing species. Journal of the Elisha Mitchell Scientific Society 67:267–278
Lazarus KL, James TY (2015) Surveying the biodiversity of the Cryptomycota using a targeted PCR approach. Fungal Ecol 14:62–70
Le Calvez T, Burgaud G, Mahé S, Barbier G, Vandenkoornhuyse P (2009) Fungal diversity in deep-sea hydrothermal ecosystems. Appl Environ Microbiol 75:6415– 6421. https://doi.org/10.1128/AEM.00653-09
Lepelletier F, Karpov SA, Alacid E, Le Panse S, Bigeard E, Garcés E, Jeanthon C, Guillou L (2014b) Dinomyces arenysensis gen. et sp. nov. (Rhizophydiales, Dinomyceataceae fam. nov.), a chytrid infecting marine dinoflagellates. Protist 165:230–244
Lepelletier F, Karpov SA, Le Panse S, Bigeard E, Skovgaard A, Jeanthon C, Guillou L (2014a) Parvilucifera rostrata sp. nov. (Perkinsozoa), a novel parasitoid that infects planktonic dinoflagellates. Protist 165:31–49
Leshem T, Letcher PM, Powell MJ, Sukenik A (2016) Characterization of a new chytrid species parasitic on the dinoflagellate, Peridinium gatunense. Mycologia 108:731–743
Letcher PM, Powell MJ (2012) A taxonomic summary and revision of Rhizophydium (Rhizophydiales, Chytridiomycota). Alabama University printing, no. 1. Imprint Tuscaloosa, AL
Letcher PM, Powell MJ, Davis WJ (2015) A new family and four new genera in Rhizophydiales (Chytridiomycota). Mycologia 107:808–830
Letcher PM, Velez CG, Barrantes ME, Powell MJ, Churchill PA, Wakefield WS (2008) Ultrastructural and molecular analyses of Rhizophydiales (Chytridiomycota) isolates from North America and Argentina. Mycol Res 112:759–782
Picard KT, Letcher PM, Powell MJ (2009) Rhizidium phycophilum, a new species in Chytridiales. Mycologia 101:696–706
Picard KT (2017) Coastal marine habitats harbor novel early-diverging fungal diversity. Fungal Ecol 25:1–13
Powell MJ (1974) Fine structure of plasmodesmata in a chytrid. Mycologia 66:606–614
Powell MJ (2016) Chytridiomycota. In: Archibald et al. (ed.), Handbook of the Protists. Springer International Publishing, Cham, Switzerland, pp 1–36
Powell MJ, Gillette L (1987) Septal structure of the chytrid Rhizophlyctis harderi. Mycologia 79:635–639
Reñé A, Alacid E, Figueroa RI, Rodríguez F, Garcés E (2017) Life-cycle, ultrastructure, and phylogeny of Parvilucifera corolla sp. nov. (Alveolata, Perkinsozoa), a parasitoid of dinoflagellates. Europ J Prot 58:9–25
Richards TA, Leonard G, Mahé F, del Campo J, Romac S, Jones MDM, Maguire F, Dunthorn M, De Vargas C, Massana R, Chambouvet A (2015) Molecular diversity and distribution of marine fungi across 130 European environmental samples. Proc Biol Sci 282:2015–2243. https://doi.org/10.1098/rspb.2015.2243
Richards TA, Jones MDM, Leonard G, Bass D (2012) Marine fungi: their ecology and molecular diversity. Annu Rev Mar Sci 4:495–522. https://doi.org/10.1146/annurev-marine-120710-100802
Scholin CA, Herzog M, Sogin M, Anderson DM (1994) Identification of group- and strain-specific genetic markers for globally distributed Alexandrium (Dinophyceae). II. Sequence analysis of a fragment of the 28S rDNA. J Phycol 30:999–1011
Scholz B, Guillou L, Marano AV, Neuhauser S, Sullivan BK, Karsten U, Küpper FC, Gleason FH (2016) Zoosporic parasites infecting marine diatoms – a black box that needs to be opened. Fungal Ecol 19:59–76
Taylor JW, Fuller MS (1981) The Golgi apparatus, zoosporogenesis, and development of the zoospore discharge apparatus of Chytridium confervae. Exp Mycol 5:35–59
Van den Wyngaert S, Seto K, Rojas-Jimenez K, Kagami M, Grossart H-S (2017) A new parasitic chytrid, Staurastromyces oculus (Rhizophydiales, Staurastromycetaceae fam. nov.), infecting the freshwater desmis Staurastrum sp. Protist 168:392–407
White TJ, Bruns T, Lee SJWT, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications 18:315–322
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.
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
All authors are sure that all data and materials as well as software application or custom code support their published claims and comply with field standards.
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Section Editor: Marco Thines
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
(DOCX 26 kb)
Supplementary Table S2
(DOCX 35.7 kb)
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11557-020-01652-x