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Molecular phylogeny and new light microscopic data of Metchnikovella spiralis (Microsporidia: Metchnikovellidae), a hyperparasite of eugregarine Polyrhabdina sp. from the polychaete Pygospio elegans

Published online by Cambridge University Press:  12 April 2021

Ekaterina V. Frolova
Affiliation:
Laboratory of Cytology of Unicellular Organisms, Institute of Cytology RAS, Tikhoretsky ave. 4, Saint Petersburg194064, Russian Federation Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya emb. 7/9, Saint Petersburg199034, Russian Federation
Gita G. Paskerova
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya emb. 7/9, Saint Petersburg199034, Russian Federation
Alexey V. Smirnov
Affiliation:
Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya emb. 7/9, Saint Petersburg199034, Russian Federation
Elena S. Nassonova*
Affiliation:
Laboratory of Cytology of Unicellular Organisms, Institute of Cytology RAS, Tikhoretsky ave. 4, Saint Petersburg194064, Russian Federation Department of Invertebrate Zoology, Faculty of Biology, Saint Petersburg State University, Universitetskaya emb. 7/9, Saint Petersburg199034, Russian Federation
*
Author for correspondence: Elena S. Nassonova, E-mail: [email protected]; [email protected]

Abstract

Metchnikovellids are a deep-branching group of microsporidia, parasites of gregarines inhabiting the alimentary tract of polychaetes and some other invertebrates. The diversity and phylogeny of these hyperparasites remain poorly studied. Modern descriptions and molecular data are still lacking for many species. The results of a light microscopy study and molecular data for Metchnikovella spiralis Sokolova et al., 2014, a hyperparasite of the eugregarine Polyrhabdina sp., isolated from the polychaete Pygospio elegans, were obtained. The original description of M. spiralis was based primarily on the analysis of stained preparations and transmission electron microscopy images. Here, the species description was complemented with the results of in vivo observations and phylogenetic analysis based on the SSU rRNA gene. It was shown that in this species, free sporogony precedes sac-bound sporogony, as it occurs in the life cycle of most other metchnikovellids. Spore sacs are entwined with spirally wound cords, and possess only one polar plug. Phylogenetic analyses did not group M. spiralis with M. incurvata, another metchnikovellid from the same gregarine species, but placed it as a sister branch to Amphiacantha. The paraphyletic nature of the genus Metchnikovella was discussed. The taxonomic summary for M. spiralis was emended.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Bass, D, Czech, L, Williams, BAP, Berney, C, Dunthorn, M, Mahé, F, Torruella, G, Stentiford, GD and Williams, TA (2018) Clarifying the relationships between microsporidia and cryptomycota. Journal of Eukaryotic Microbiology 65, 773782.CrossRefGoogle ScholarPubMed
Batson, BS (1982) A light and electron microscopical study of Trichoduboscqia epeori Léger (Microspora: Duboscqiidae). The Journal of Protozoology 29, 202212.CrossRefGoogle Scholar
Caullery, M and Mesnil, F (1914) Sur les Metchnikovellidae et autres Protistes parasites des Grégarines d'Annélides. Comptes Rendus de Seances de la Societe de Biologie, Paris 77, 527532.Google Scholar
Caullery, M and Mesnil, F (1919) Metchnikovellidae et autres Protistes parasites des Grégarines d’ Annélides. Annales de l'Institut Pasteur 33, 209240.Google Scholar
Corsaro, D, Michel, R, Walochnik, J, Venditti, D, Müller, KD, Hauröder, B and Wylezich, C (2016) Molecular identification of Nucleophaga terricolae sp. nov. (Rozellomycota), and new insights on the origin of the Microsporidia. Parasitology Research 115, 30033011.CrossRefGoogle Scholar
Corsaro, D, Wylezich, C, Venditti, D, Michel, R, Walochnik, J and Wegensteiner, R (2018) Filling gaps in the microsporidian tree: rDNA phylogeny of Chytridiopsis typographi (Microsporidia: Chytridiopsida). Parasitology Research 118, 169180.CrossRefGoogle Scholar
Corsaro, D, Walochnik, J, Venditti, D, Hauröder, B and Michel, R (2020) Solving an old enigma: Morellospora saccamoebae gen. nov., sp. nov. (Rozellomycota), a Sphaerita-like parasite of free-living amoebae. Parasitology Research 119, 925934.CrossRefGoogle Scholar
Desportes, I and Théodoridès, J (1979) Étude ultrastructurale d’Amphiamblys laubieri n. sp. (Microsporidie, Metchnikovellidae) parasite d'une Grégarine (Lecudina sp.) d'un Echiurien abyssal. Protistologica 15, 435457.Google Scholar
Dogiel, VA (1922) Sur un nouveau genre de Metchnikovellidae. Annales de l'Institut Pasteur 36, 574577.Google Scholar
Edgar, RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32, 17921797.CrossRefGoogle ScholarPubMed
Galindo, LJ, Torruella, G, Moreira, D, Timpano, H, Paskerova, G, Smirnov, A, Nassonova, E and López-García, P (2018) Evolutionary genomics of Metchnikovella incurvata (Metchnikovellidae): an early branching microsporidium. Genome Biology and Evolution 10, 27362748.CrossRefGoogle ScholarPubMed
Gouy, M, Guindon, S and Gascuel, O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Molecular Biology and Evolution 27, 221224.CrossRefGoogle ScholarPubMed
Grossart, H-P, Wurzbacher, C, James, TY and Kagami, M (2016) Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi. Fungal Ecology 19, 2838.CrossRefGoogle Scholar
Hildebrand, HF (1974) Observations ultrastructurales sur le stade plasmodial de Metchnikovella wohlfarthi Hildebrand et Vivier 1971, Microsporidie hyperparasite de la Grégarine Lecudina tuzetae. Protistologica 10, 515.Google Scholar
Hildebrand, H and Vivier, E (1971) Observations ultrastructurales sur le sporoblaste de Metchnikovella wohlfarthi n. sp. (Microsporidies), parasite de la grégarine Lecudina tuzetae. Protistologica 7, 131139.Google Scholar
Ishida, S, Nozaki, D, Grossart, HP and Kagami, M (2015) Novel basal, fungal lineages from freshwater phytoplankton and lake samples. Environmental Microbiology Reports 7, 435441.CrossRefGoogle ScholarPubMed
Larsson, JR (1994) Trichoctosporea pygopellita gen. et sp. nov. (Microspora, Thelohaniidae), a microsporidian parasite of the mosquito Aedes vexans (Diptera, Culicidae). Archiv für Protistenkunde 144, 147161.CrossRefGoogle Scholar
Larsson, JR (2000) The hyperparasitic microsporidium Amphiacantha longa Caullery et Mesnil, 1914 (Microspora: Metchnikovellidae) – description of the cytology, redescription of the species, emended diagnosis of the genus Amphiacantha and establishment of the new family Amphiacanthidae. Folia Parasitologica 47, 241256.CrossRefGoogle ScholarPubMed
Larsson, JIR (2014) The primitive microsporidia. In Weiss, LM and Becnel, JJ (eds), Microsporidia: Pathogens of Opportunity. Hoboken, New Jersey: John Wiley and Sons, Inc, pp. 605634. doi: 10.1002/9781118395264.ch24Google Scholar
Larsson, JR and Køie, M (2006) The ultrastructure and reproduction of Amphiamblys capitellides (Microspora, Metchnikovellidae), a parasite of the gregarine Ancora sagittata (Apicomplexa, Lecudinidae), with redescription of the species and comments on the taxonomy. European Journal of Protistology 42, 233248.CrossRefGoogle Scholar
Larsson, JIR and Voronin, VN (2000) Light and electron microscopic study of Agglomerata volgensae n. sp. (Microspora: Dubosqiidae), a new microsporidian parasite of Daphnia magna (Crustacea: Daphniidae). European Journal of Protistology 36, 8999.CrossRefGoogle Scholar
Lazarus, KL and James, TY (2015) Surveying the biodiversity of the Cryptomycota using a targeted PCR approach. Fungal Ecology 14, 6270.CrossRefGoogle Scholar
Mikhailov, KV, Simdyanov, TG and Aleoshin, VV (2017) Genomic survey of a hyperparasitic microsporidian Amphiamblys sp. (Metchnikovellidae). Genome Biology and Evolution 9, 454467.Google Scholar
Mikhailov, KV, Nassonova, ES, Shishkin, YA, Paskerova, GG, Simdyanov, TG, Yudina, VA, Smirnov, AV, Janouškovec, J and Aleoshin, VV (2021) Ribosomal RNA of the metchnikovellids in gregarine transcriptomes and rDNA of the microsporidia sensu lato in environmental metagenomes. Zhurnal Obshchei Biologii 82. doi: 10.31857/S0044459621030040 (in Russian with English summary).Google Scholar
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE). Presented at the 2010 Gateway Computing Environments Workshop (GCE), IEEE, New Orleans, LA, USA, pp. 18. doi: 10.1109/GCE.2010.5676129.CrossRefGoogle Scholar
Nagahama, T, Takahashi, E, Nagano, Y, Abdel-Wahab, MA and Miyazaki, M (2011) Molecular evidence that deep-branching fungi are major fungal components in deep-sea methane cold-seep sediments. Environmental Microbiology 13, 23592370.CrossRefGoogle ScholarPubMed
Nassonova, ES, Bondarenko, NI, Paskerova, GG, Kováčiková, M, Frolova, EV and Smirnov, AV (2021) Evolutionary relationships of Metchnikovella dogieli Paskerova et al., 2016 (Microsporidia: Metchnikovellidae) revealed by multigene phylogenetic analysis. Parasitology Research 120, 525534.CrossRefGoogle ScholarPubMed
Ormières, R, Loubès, C and Maurand, J (1981) Amphiamblys bhatiellae n. sp., Microsporidie parasite de Bhatiella marphysae Setna, 1931, Eugrégarine d'Annelide Polychète. Protistologica 17, 273280.Google Scholar
Richards, TA, Leonard, G, Mahé, F, Del Campo, J, Romac, S, Jones, MD, Maguire, F, Dunthorn, M, De Vargas, C, Massana, R and Chambouvet, A (2015) Molecular diversity and distribution of marine fungi across 130 European environmental samples. Proceedings of the Royal Society B: Biological Sciences 282, 20152243.CrossRefGoogle ScholarPubMed
Ronquist, F, Teslenko, M, Van Der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.CrossRefGoogle ScholarPubMed
Rotari, YM (1988) Microsporidia-hyperparasites of the White Sea polychaetes (MS Dissertation), Biological Science, Dept. Invertebrate Zoology. Leningrad State University, Leningrad.Google Scholar
Rotari, Y and Paskerova, G (2007) New data on hyperparasitic microsporidians from polychaetes of the White Sea. Protistology 5, 6768.Google Scholar
Rotari, YM, Paskerova, GG and Sokolova, YY (2015) Diversity of metchnikovellids (Metchnikovellidae, Rudimicrosporea), hyperparasites of bristle worms (Annelida, Polychaeta) from the White Sea. Protistology 9, 5059.Google Scholar
Sokolova, YY, Paskerova, GG, Rotari, YM, Nassonova, ES and Smirnov, AV (2013) Fine structure of Metchnikovella incurvata Caullery and Mesnil, 1914 (Microsporidia), a hyperparasite of gregarines Polyrhabdina sp. from the polychaete Pygospio elegans. Parasitology 140, 855867.CrossRefGoogle Scholar
Sokolova, Y, Paskerova, G, Rotari, Y, Nassonova, E and Smirnov, A (2014) Description of Metchnikovella spiralis sp. n. (Microsporidia: Metchnikovellidae), with notes on the ultrastructure of metchnikovellids. Parasitology 141, 11081122.CrossRefGoogle Scholar
Sprague, V (1977) Classification and phylogeny of microsporidia. In Bulla, LA and Cheng, TC (eds), Comparative Pathobiology, vol. 2. New York, USA: Plenum Press, pp. 130.Google Scholar
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 13121313.CrossRefGoogle ScholarPubMed
Stentiford, GD, Ramilo, A, Abollo, E, Kerr, R, Bateman, KS, Feist, SW, Bass, D and Villalba, A (2017) Hyperspora aquatica n.gn., n.sp. (Microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microspordian taxa. Parasitology 144, 186199.CrossRefGoogle Scholar
Vávra, J and Larsson, JIR (2014) Structure of microsporidia. In Weiss, LM and Becnel, JJ (eds), Microsporidia: Pathogens of Opportunity. Hoboken, New Jersey: John Wiley and Sons, Inc, pp. 170. doi: 10.1002/9781118395264.ch1.Google Scholar
Vivier, E (1975) The microsporidia of the protozoa. Protistologica 11, 345361.Google Scholar
Vivier, E and Schrével, J (1973) Étude en microscopie photonique et électronique de différents stades du cycle de Metchnikovella hovassei et observations sur la position systématique des Metchnikovellidae. Protistologica 9, 95118.Google Scholar
Vossbrinck, CR, Debrunner-Vossbrinck, BA and Weiss, LM (2014) Phylogeny of the microsporidia. Microsporidia: Pathogens of Opportunity. Hoboken, New Jersey: John Wiley and Sons, Inc, pp. 203220. doi: 10.1002/9781118395264.ch6.Google Scholar
Weiser, J (1977) Contribution to the classification of microsporidia. Vestnik Ceskoslovenske Spolecnosti Zoologicke 41, 308321.Google Scholar
Weiss, LM and Vossbrinck, CR (1999) Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the microsporidia. In Wittner, M and Weiss, L (eds), The Microsporidia and Microsporidiosis. American Society of Microbiologists. Washington, DC: ASM Press, pp. 129171. doi: 10.1128/9781555818227.ch4.Google Scholar
Williams, BAP, Hamilton, KM, Jones, MD and Bass, D (2018) Group-specific environmental sequencing reveals high levels of ecological heterogeneity across the microsporidian radiation: ecological heterogeneity in the microsporidia. Environmental Microbiology 10, 328336.Google Scholar