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Evolutionary relationships of Metchnikovella dogieli Paskerova et al., 2016 (Microsporidia: Metchnikovellidae) revealed by multigene phylogenetic analysis

  • Genetics, Evolution, and Phylogeny - Original Paper
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Abstract

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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Data availability

The dataset used in this study is deposited with the GeneBank under the accession numbers: MT969020 (SSU rDNA), MT951446, MW052334-MW052379 (protein-coding genes).

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Acknowledgements

The authors thank the staff of the White Sea Biological Station of M. V. Lomonosov Moscow State University for providing facilities for field sampling and material processing, as well as for their kind and friendly approach. The authors also thank Guifré Torruella, Luis Javier Galindo, Hélène Timpano, David Moreira, and Purificación López-García (Ecologie Systématique Evolution, CNRS, Université Paris-Sud, AgroParisTech, Université Paris-Saclay, Orsay, France) for the alignments of conserved single-copy protein domains used for the phylogenomic analysis and for sharing their expertise in performing of single-cell genomics. This study utilised equipment of the Core Facility Centres ‘Biobank’, ‘Development of Molecular and Cell Technologies’, and ‘Culture Collection of Microorganisms’ of the Research Park of Saint Petersburg State University.

Funding

This study was financially supported by the Russian Science Foundation—project no. 19-74-20136 (phylogenetic analyses, bioinformatics and data treatment) and by the Russian Foundation for Basic Research—projects no. 18-04-01359 (light microscopy, molecular work, NGS sequencing). Financial support for fieldwork of GP was provided in part by St. Petersburg State University—grant no. 1.42.1099.2016. The fieldwork of MK was supported by the Czech Science Foundation, project no. GBP505/12/G112 (ECIP).

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Authors and Affiliations

  1. Laboratory of Cytology of Unicellular Organisms, Institute of Cytology RAS, Tikhoretsky ave. 4, St. Petersburg, Russia, 194064

    Elena S. Nassonova, Natalya I. Bondarenko & Ekaterina V. Frolova

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

    Elena S. Nassonova, Natalya I. Bondarenko, Gita G. Paskerova, Ekaterina V. Frolova & Alexey V. Smirnov

  3. Department of Botany and Zoology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37, Brno, Czech Republic

    Magdaléna Kováčiková

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  1. Elena S. Nassonova
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  3. Gita G. Paskerova
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Contributions

Elena Nassonova and Alexey Smirnov suggested an overall concept and design of the study, performed molecular phylogeny and phylogenomics, and drafted the manuscript; Gita Paskerova, Ekaterina Frolova, and Magdaléna Kováčiková performed the field work, dissections of polychaetes, and isolation of the parasites; Alexey Smirnov and Gita Paskerova did light microscopy and single-cell manipulations; Elena Nassonova conducted molecular studies; Natalya Bondarenko performed bioinformatic treatment of NGS data. All authors contributed to the improvement of the draft and accepted the final version of the manuscript.

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Correspondence to Elena S. Nassonova.

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This article does not contain any studies with human participants or warm-blooded animals performed by any of the authors. The White Sea Biological Station of M. V. Lomonosov Moscow State University has permission to collect invertebrate animals for scientific work on its own territory and other sites situated around the station. The invertebrates of interest are neither endangered nor protected species within the region. Animal handling and dissecting was performed at cold temperature to avoid distress and unnecessary suffering.

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Code availability (software application or custom code)

FastQC http://www.bioinformatics.babraham.ac.uk/projects/fastqc/

Trimmomatic http://www.usadellab.org/cms/?page=trimmomatic

SPAdes v.3.13.0 http://cab.spbu.ru/files/release3.13.0/manual.html

QUAST http://cab.spbu.ru/software/quast/

SAMtools http://samtools.sourceforge.net

SeaView 4.6.1 http://doua.prabi.fr/software/seaview

BLASTx https://blast.ncbi.nlm.nih.gov/Blast.cgi?LINK_LOC=blasthome&PAGE_TYPE=BlastSearch&PROGRAM=blastx

RAxML-HPC2 on XSEDE (v.8.2.12) https://www.phylo.org

MrBayes v.3.2.6 http://www.phylo.org

PhyloBayes MPI on XSEDE (v.1.4f) http://www.phylo.org/tools/obsolete/phylobayes_xsede.html

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Nassonova, E.S., Bondarenko, N.I., Paskerova, G.G. et al. Evolutionary relationships of Metchnikovella dogieli Paskerova et al., 2016 (Microsporidia: Metchnikovellidae) revealed by multigene phylogenetic analysis. Parasitol Res 120, 525–534 (2021). https://doi.org/10.1007/s00436-020-06976-x

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