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Analysis of major sperm proteins in two nematode species from two classes, Enoplus brevis (Enoplea, Enoplida) and Panagrellus redivivus (Chromadorea, Rhabditida), reveals similar localization, but less homology of protein sequences than expected for Nematoda phylum

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Abstract

Major sperm proteins (MSPs) are a nematode-specific system of cytoskeletal proteins required for amoeboid sperm movement. A number of MSP genes vary in different nematode species, but encoded protein sequences reveal high homology between these proteins. However, all studies of MSP localization and functions to date are based exclusively on the representatives of the order Rhabditida belonging to the nematode class Chromadorea, while MSP-driven sperm movement in Enoplea, another major clade of the phylum Nematoda is still unconfirmed. In this study, we documented the presence of MSPs in the enoplean nematode Enoplus brevis (Bastian, 1865) (Enoplida) and compared MSP localization in sperm of this species with that of the chromadorean nematode Panagrellus redivivus (Linnaeus, 1767) (Rhabditida). Then, we analyzed the putative MSP sequences of both species. Our results indicate that MSPs are presented in E. brevis spermatozoa and form filamentous structures after sperm activation, which may be considered as the evidence of their motor functions similar to those in the spermatozoa of chromadorean nematodes. We found that E. brevis MSPs show lower homology to known proteins of rhabditids whose species exhibit hyper-conservatism in MSP protein sequences. These results reflect the more distant evolutionary relationships between Enoplea and Chromadorea than exist within Rhabditida order. Our data reveal a need to reevaluate current views of MSP evolution within Nematoda.

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Data availability

Nucleotide sequences coding E. brevis MSP124-1, MSP124-2, and MSP124-3 were deposited to the Third Party Annotation Section of the DDBJ/ENA/GenBank databases under the accession numbers TPA: BK014294-BK014296.

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Acknowledgements

The authors are grateful to staff of the Far Eastern Center of Electron Microscopy (NSCMB FEB RAS) for their assistance in imaging and to staff of the White Sea Biological Station (Lomonosov Moscow State University) for the help in E. brevis collection. The authors are also thankful for the copyright permissions to use previously published data from the Russian Journal of Nematology (Fig. 3a and Fig. S1a) and the Fundamental and Applied Nematology (Brill) (Fig. 6b and Fig. S2).

Funding

This study was supported by Russian Foundation for Basic Research (Grant Nos. 17–04-00719-a and 14–04-00334-a).

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Correspondence to Konstantin V. Yakovlev.

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Zograf, J.K., Trebukhova, Y.A., Yushin, V.V. et al. Analysis of major sperm proteins in two nematode species from two classes, Enoplus brevis (Enoplea, Enoplida) and Panagrellus redivivus (Chromadorea, Rhabditida), reveals similar localization, but less homology of protein sequences than expected for Nematoda phylum. Org Divers Evol 22, 117–130 (2022). https://doi.org/10.1007/s13127-021-00522-y

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  • DOI: https://doi.org/10.1007/s13127-021-00522-y

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