Evolutionary relationships of Metchnikovella dogieli Paskerova et al., 2016 (Microsporidia: Metchnikovellidae) revealed by multigene phylogenetic analysis
Language English Country Germany Media print-electronic
Document type Journal Article
Grant support
19-74-20136
Russian Science Foundation (RSF) (RU)
18-04-01359
Russian Foundation for Basic Research (RFBR) (RU)
PubMed
33415389
DOI
10.1007/s00436-020-06976-x
PII: 10.1007/s00436-020-06976-x
Knihovny.cz E-resources
- Keywords
- Metchnikovellids, Microsporidia, Phylogenomics, Phylogeny,
- MeSH
- Apicomplexa microbiology MeSH
- Phylogeny MeSH
- Genomics MeSH
- Microsporidia classification genetics ultrastructure MeSH
- Evolution, Molecular MeSH
- Polychaeta parasitology MeSH
- Spores, Fungal ultrastructure MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Geographicals
- Russia MeSH
The species Metchnikovella dogieli (Paskerova et al. Protistology 10:148-157, 2016) belongs to one of the early diverging microsporidian groups, the metchnikovellids (Microsporidia: Metchnikovellidae). In relation to typical ('core') microsporidia, this group is considered primitive. The spores of metchnikovellids have no classical polar sac-anchoring disk complex, no coiled polar tube, no posterior vacuole, and no polaroplast. Instead, they possess a short thick manubrium that expands into a manubrial cistern. These organisms are hyperparasites; they infect gregarines that parasitise marine invertebrates. M. dogieli is a parasite of the archigregarine Selenidium pygospionis (Paskerova et al. Protist 169:826-852, 2018), which parasitises the polychaete Pygospio elegans. This species was discovered in samples collected in the silt littoral zone at the coast of the White Sea, North-West Russia, and was described based on light microscopy. No molecular data are available for this species, and the publicly accessible genomic data for metchnikovellids are limited to two species: M. incurvata Caullery & Mesnil, 1914 and Amphiamblys sp. WSBS2006. In the present study, we applied single-cell genomics methods with whole-genome amplification to perform next-generation sequencing of M. dogieli genomic DNA. We performed a phylogenetic analysis based on the SSU rRNA gene and reconstructed a multigene phylogeny using a concatenated alignment that included 46 conserved single-copy protein domains. The analyses recovered a fully supported clade of metchnikovellids as a basal group to the core microsporidia. Two members of the genus Metchnikovella did not form a clade in our tree. This may indicate that this genus is paraphyletic and requires revision.
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Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25(17):3389–3402. https://doi.org/10.1093/nar/25.17.3389 PubMed DOI PMC
Bankevich A, Nurk S, Antipov D, Gurevich A, Dvorkin M, Kulikov AS, Lesin V, Nikolenko S, Pham S, Prjibelski A, Pyshkin A, Sirotkin A, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021 PubMed DOI PMC
Bass D, Czech L, Williams BAP, Berney C, Dunthorn M, Mahé F, Torruella G, Stentiford GD, Williams TA (2018) Clarifying the relationships between microsporidia and cryptomycota. J Eukaryot Microbiol 65:773–782. https://doi.org/10.1111/jeu.12519 PubMed DOI PMC
Becnel JJ, Takvorian PM, Cali A (2014) Checklist of available generic names for Microsporidia with type species and type hosts. In: Weiss LM, Becnel JJ (eds) Microsporidia: pathogens of opportunity. John Wiley & Sons, Inc., Ames, Iowa, pp 671–686. https://doi.org/10.1002/9781118395264.app1 DOI
Cali A, Becnel JJ, Takvorian PM (2017) Microsporidia. In: Archibald JM et al (eds) Handbook of the protists, 2nd edn. Springer, Cham, Switzerland, pp 1559–1618. https://doi.org/10.1007/978-3-319-28149-0_27 DOI
Canning E, Vávra J (2000) Phylum Microsporida Balbiani, 1882. In: Lee JJ et al (eds) An illustrated guide to the protozoa: organisms traditionally referred to as protozoa, or newly discovered groups, vol 1, 2nd edn. Allen Press, Lawrence, Kan, pp 39–126
Caullery M, Mesnil F (1897) Sur un type nouveau (Metchnikovella n.g.) d’organismes parasites des grégarines. C R Séances Soc Biol 4(49):960–962
Caullery M, Mesnil F (1914) Sur les Metchnikovellidae et autres Protistes parasites des Grégarines d’Annélides. C R Séances Soc Biol 2(77):527–532
Caullery M, Mesnil F (1919) Metchnikovellidae et autres Protistes parasites des Grégarines d’ Annélides. Ann Inst Pasteur 33(4):209–240
Corsaro D, Michel R, Walochnik J, Venditti D, Müller KD, Hauröder B, Wylezich C (2016) Molecular identification of Nucleophaga terricolae sp. nov. (Rozellomycota), and new insights on the origin of the Microsporidia. Parasitol Res 115:3003–3011. https://doi.org/10.1007/s00436-016-5055-9 PubMed DOI
Corsaro D, Wylezich C, Venditti D, Michel R, Walochnik J, Wegensteiner R (2018) Filling gaps in the microsporidian tree: rDNA phylogeny of Chytridiopsis typographi (Microsporidia: Chytridiopsida). Parasitol Res 118(1):169–180. https://doi.org/10.1007/s00436-018-6130-1 PubMed DOI
Corsaro D, Walochnik J, Venditti D, Hauröder B, Michel R (2020) Solving an old enigma: Morellospora saccamoebae gen. nov., sp. nov. (Rozellomycota), a Sphaerita-like parasite of free-living amoebae. Parasitol Res 119(3):925–934. https://doi.org/10.1007/s00436-020-06623-5 PubMed DOI
Desportes I, Théodoridès J (1979) Étude ultrastructurale d’Amphiamblys laubieri n. sp. (Microsporidie, Metchnikovellidae) parasite d’une Grégarine (Lecudina sp.) d’un Echiurien abyssal. Protistologica 15:435–457
Dogiel VA (1922) Sur un nouveau genre de Metchnikovellidae. Ann Inst Pasteur 36:574–577
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340 PubMed DOI PMC
Galindo LJ, Torruella G, Moreira D, Timpano H, Paskerova G, Smirnov A, Nassonova E, López-García P (2018) Evolutionary genomics of Metchnikovella incurvata (Metchnikovellidae): an early branching microsporidium. Genome Biol Evol 10:2736–2748. https://doi.org/10.1093/gbe/evy205 PubMed DOI PMC
Gouy M, Guindon S, Gascuel O (2010) SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224. https://doi.org/10.1093/molbev/msp259 DOI
Grossart H-P, Wurzbacher C, James TY, Kagami M (2016) Discovery of dark matter fungi in aquatic ecosystems demands a reappraisal of the phylogeny and ecology of zoosporic fungi. Fungal Ecol 19:28–38. https://doi.org/10.1016/j.funeco.2015.06.004 DOI
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59(3):307–321. https://doi.org/10.1093/sysbio/syq010 PubMed DOI
Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075. https://doi.org/10.1093/bioinformatics/btt086 PubMed DOI PMC
Issi IV (1986) Microsporidia as a phylum of parasitic protozoa. In: Beyer TV and Issi IV (eds) Microsporidia. Series Protozoologiya, Vol 10, Nauka, Leningrad, pp 6–136 (in Russian with English summary)
Issi IV, Voronin VN (2007) Phylum Microsporidia Balbiani 1882. In: Frolov AO and Krylov MV (eds) Protista: handbook on zoology. Pt 2, Nauka, St. Petersburg, pp 994–1045 (in Russian with English summary)
Keeling PJ, Fast NM, Corradi N (2014) Microsporidian genome structure and function. In: Weiss LM, Becnel JJ (eds) Microsporidia: pathogens of opportunity. John Wiley & Sons, Inc., Ames, Iowa, pp 221–229. https://doi.org/10.1002/9781118395264.ch7 DOI
Larsson JIR (2014) The primitive microsporidia. In: Weiss LM, Becnel JJ (eds) Microsporidia pathogens of opportunity. John Wiley & Sons, Inc., Ames, Iowa, pp 605–634. https://doi.org/10.1002/9781118395264.ch24 DOI
Lartillot N, Philippe H (2004) A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol Biol Evol 21(6):1095–1109. https://doi.org/10.1093/molbev/msh112 PubMed DOI
Lazarus KL, James TY (2015) Surveying the biodiversity of the Cryptomycota using a targeted PCR approach. Fungal Ecol 14:62–70. https://doi.org/10.1016/j.funeco.2014.11.004 DOI
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map (SAM) format and SAMtools. Transplant Proc 19:1653–1654. https://doi.org/10.1093/bioinformatics/btp352 DOI
Mikhailov KV, Simdyanov TG, Aleoshin VV (2017) Genomic survey of a hyperparasitic microsporidian Amphiamblys sp. (Metchnikovellidae). Genome Biol Evol 9:454–467. https://doi.org/10.1093/gbe/evw235 PubMed DOI
Miller MA, Pfeiffer W, 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. 1–8. https://doi.org/10.1109/GCE.2010.5676129
Nassonova E, Moreira D, Torruella G, Timpano H, Paskerova G, Smirnov A, Lopez-Garcia P (2016) Phylogenomic insights on the evolution of metchnikovellids. Protistology 10:52
Ormières R, Loubès C, Maurand J (1981) Amphiamblys bhatiellae n. sp., Microsporidie parasite de Bhatiella marphysae Setna, 1931, Eugrégarine d’Annelide Polychète. Protistologica 17:273–280
Paskerova GG, Frolova EV, Kováčiková M, Panfilkina TS, Mesentsev YS, Smirnov AV, Nassonova ES (2016) Metchnikovella dogieli sp. n. (Microsporidia: Metchnikovellida), a parasite of archigregarines Selenidium sp. from polychaetes Pygospio elegans. Protistology 10(4):148–157. https://doi.org/10.21685/1680-0826-2016-10-4-4 DOI
Paskerova GG, Miroliubova TS, Diakin A, Kováčiková M, Valigurová A, Guillou L, Aleoshin VV, Simdyanov TG (2018) Fine structure and molecular phylogenetic position of two marine gregarines, Selenidium pygospionis sp. n. and S. pherusae sp. n., with notes on the phylogeny of Archigregarinida (Apicomplexa). Protist 169(6):826–852. https://doi.org/10.1016/j.protis.2018.06.004 PubMed DOI
Reichenow E (1932) Sporozoa. In: Grimpe G and Wagler E (eds) Die Tierwelt der Nord- und Ostsee. 21(II). Leipzig, Akademische Verlagsgesellschaft, g1–g48
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. https://doi.org/10.1093/sysbio/sys029 PubMed DOI PMC
Schereschevsky H (1924) La famille Metchnikovellidae (C.& M.) et la place qu’elle occupe dans le Systéms de Protistes. Arch Russ Protistol 3:137–145 (in Russian with French summary)
Schrével J, Desportes I (2013) Biology of gregarines and their host-parasite interactions. Ch 2 in: Desportes I and Schrével J (eds) Treatise on zoology–anatomy, taxonomy, biology. The gregarines. BRILL, Leiden, Boston, pp 25–195. https://doi.org/10.1163/9789004256057_004
Sokolova YY, Paskerova GG, Rotari YM, Nassonova ES, 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 140:855–867. https://doi.org/10.1017/S0031182013000036 PubMed DOI
Sprague V (1977) Classification and phylogeny of microsporidia. In: Bulla LA, Cheng TC (eds) Comparative pathobiology, vol 2. Plenum Press, New York, pp 1–30
Sprague V, Becnel JJ, Hazard EI (1992) Taxonomy of phylum Microspora. Crit Rev Microbiol 18(5–6):285–395. https://doi.org/10.3109/10408419209113519 PubMed DOI
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033 PubMed DOI PMC
Stentiford GD, Ramilo A, Abollo E, Kerr R, Bateman KS, Feist SW, Bass D, Villalba A (2017) Hyperspora aquatica n.gn., n.sp. (Microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microspordian taxa. Parasitology 144:186–199. https://doi.org/10.1017/S0031182016001633 PubMed DOI
Stubblefield JW (1955) The morphology and life history of Amphiacantha ovalis and A. attenuata, two new haplosporidian parasites of gregarines. J Parasitol 41(5):443–459 DOI
Talavera G, Castresana J (2007) Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56:564–577. https://doi.org/10.1080/10635150701472164 PubMed DOI
Torruella G, Derelle R, Paps J, Lang BF, Roger AJ, Shalchian-Tabrizi K, Ruiz-Trillo I (2012) Phylogenetic relationships within the Opisthokonta based on phylogenomic analyses of conserved single-copy protein domains. Mol Biol Evol 29(2):531–544. https://doi.org/10.1093/molbev/msr185 PubMed DOI
Vávra J, Larsson JIR (2014) Structure of Microsporidia. In: Weiss LM, Becnel JJ (eds) Microsporidia pathogens of opportunity. John Wiley & Sons, Inc., Ames, Iowa, pp 1–70. https://doi.org/10.1002/9781118395264.ch1 DOI
Vávra J, Lukeš J (2013) Microsporidia and ‘the art of living together’. In: Rollinson D (ed) Advances in parasitology. Academic Press, pp 253–319. https://doi.org/10.1016/B978-0-12-407706-5.00004-6
Vivier E (1975) The Microsporidia of the Protozoa. Protistologica 11(3):345–361
Vivier E, 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 9:95–118
Vossbrinck CR, Debrunner-Vossbrinck BA, Weiss LM (2014) Phylogeny of the Microsporidia. In: Weiss LM, Becnel JJ (eds) Microsporidia: pathogens of opportunity. John Wiley & Sons, Inc., Ames, Iowa, pp 203–220. https://doi.org/10.1002/9781118395264.ch6 DOI
Weiss LM, Becnel JJ (eds) (2014) Microsporidia: pathogens of opportunity. John Wiley and Sons, Inc., Ames, Iowa. https://doi.org/10.1002/9781118395264 DOI
Weiss LM, Vossbrinck CR (1999) Molecular biology, molecular phylogeny, and molecular diagnostic approaches to the Microsporidia. In: Wittner M, Weiss L (eds) The Microsporidia and microsporidiosis. Amer Soc Microbiol, Washington D.C., pp 129–171
Williams BAP, Hamilton KM, Jones MD, Bass D (2018) Group-specific environmental sequencing reveals high levels of ecological heterogeneity across the microsporidian radiation: ecological heterogeneity in the microsporidia. Environ Microbiol 10:328–336. https://doi.org/10.1111/1758-2229.12642 DOI
Zhu X, Wittner M, Tanowitz HB, Kotler D, Cali A, Weiss LM (1993) Small subunit rRNA sequence of Enterocytozoon bieneusi and its potential diagnostic role with use of the polymerase chain reaction. J Infect Dis 168:1570–1575. https://doi.org/10.1093/infdis/168.6.1570 PubMed DOI