L31 Transposons of Hexacorallia: Distribution, Diversity and Evolution

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Abstract

Transposable elements (TE) of eukaryotes – retrotransposons and DNA transposons – are nucleotide sequences that can move from locus to locus of the genome, as well as between the genomes of different organisms. L31 DNA transposons are an ancient and diverse group belonging to the large IS630/Tc1/mariner group. L31 transposons are not widespread and are present in a limited number of taxa. In addition to the sequence encoding the DDE/D transposase, L31 transposons carry another ORF (ORF2). Detailed analysis of L31 elements in the genomes of six-rayed corals has provided detailed information on the distribution, diversity and structure of the elements. Two large groups, L31-duo and L31-uno, were identified, differing in both catalytic domain pattern and structure. As a result of reconstruction of the evolution of L31 transposons, it was suggested that six-rayed corals received L31 transposons from bivalves. At the same time, the split-off group L31-uno may have been obtained by mollusks as a result of horizontal transfer from corals. Studies of the distribution and diversity of TE in marine invertebrates will contribute to a better understanding of the evolutionary processes of TE and their role in the evolutionary history of species.

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About the authors

L. V. Puzakova

Kovalevsky Institute of Biology of the Southern Seas of Russian Academy of Sciences

Email: puzakov.mikh@yandex.ru
Russian Federation, Sevastopol, 299011

M. V. Puzakov

Kovalevsky Institute of Biology of the Southern Seas of Russian Academy of Sciences

Author for correspondence.
Email: puzakov.mikh@yandex.ru
Russian Federation, Sevastopol, 299011

P. M. Puzakova

Lomonosov Moscow State University, Branch in Sevastopol

Email: puzakov.mikh@yandex.ru
Russian Federation, Sevastopol, 299001

References

  1. Kojima K.K. Structural and sequence diversity of eukaryotic transposable elements // Genes Genet. Syst. 2020. V. 94. № 6. P. 233–252. https://doi.org/10.1266/ggs.18-00024
  2. Wells J.N., Feschotte C.A. Field guide to eukaryotic transposable elements // Annu. Rev. Genet. 2020. V. 54. P. 539–561. https://doi.org/10.1146 annurev-genet-040620-022145
  3. Wicker T., Sabot F., Hua-Van A. et al. A unified classification system for eukaryotic transposable elements // Nat. Rev. Genet. 2007. V. 8. № 12. P. 973–982. https://doi.org/10.1038/nrg2165
  4. Kapitonov V.V., Jurka J. A universal classification of eukaryotic transposable elements implemented in Repbase // Nat. Rev. Genet. 2008. V. 9. P. 411–412. https://doi.org/10.1038/nrg2165-c1
  5. Yuan Y.W., Wessler S.R. The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies // Proc. Natl Acad. Sci. USA. 2011. V. 108. № 19. P. 7884–7889. https://doi.org/10.1073/pnas.1104208108
  6. Arkhipova I.R. Using bioinformatic and phylogenetic approaches to classify transposable elements and understand their complex evolutionary histories // Mob. DNA. 2017. V. 8. № 19. https://doi.org/10.1186/s13100-017-0103-2
  7. Gao B., Wang Y.L., Diaby M. et al. Evolution of pogo, a separate superfamily of IS630-Tc1-mariner transposons, revealing recurrent domestication events in vertebrates // Mob. DNA. 2020. V. 11. № 25.
  8. Shi S., Puzakov M., Guan Z. et al. Prokaryotic and eukaryotic horizontal transfer of Sailor (dd82e), a new superfamily of IS630-Tc1-Mariner DNA-transposons // Biology (Basel). 2021. V. 10. № 10. https://doi.org/10.3390/biology10101005
  9. Puzakov M.V., Puzakova L.V. Structure and evolution of DNA transposons of the L31 superfamily in Bivalves // Mol. Biol. 2024. V. 58. № 1. P. 57–75. https://doi.org/10.1134/S0026893324010114
  10. Shi S., Puzakov M.V., Puzakova L.V. et al. Hiker, a new family of DNA transposons encoding transposases with DD35E motifs, displays a distinct phylogenetic relationship with most known DNA transposon families of IS630-Tc1-mariner (ITm) // Mol. Phylog. Evol. 2023. V. 188. https://doi.org/10.1016/j.ympev.2023.107906
  11. Aziz R.K., Breitbart M., Edwards R.A. Transposases are the most abundant, most ubiquitous genes in nature // Nucl. Ac. Res. 2010. V. 38. № 13. P. 4207–4217. https://doi.org/10.1093/nar/gkq140
  12. Puzakov M.V., Puzakova L.V., Cheresiz S.V. An Analysis of IS630/Tc1/mariner transposons in the genome of a pacific oyster Crassostrea gigas // J. Mol. Evol. 2018. V. 86. № 8. P. 566–580. https://doi.org/10.1007/s00239-018-9868-2
  13. Dupeyron M., Baril T., Bass C., Hayward A. Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements // Mob. DNA. 2020. V. 11. № 21. https://doi.org/10.1186/s13100-020-00212-0
  14. Tellier M., Bouuaert C.C., Chalmers R. Mariner and the ITm superfamily of transposons // Microbiol. Spectr. 2015. V. 3. № 2. https://doi.org/10.1128/microbiolspec.MDNA3-0033-2014
  15. Ivics Z., Izsvák Z. Sleeping Beauty transposition // Microbiol. Spectr. 2015. V. 3. № 2. https://doi.org/10.1128/microbiolspec.MDNA3-0042-2014
  16. Jahn C.L., Doktor S.Z., Frels J.S. et al. Structures of the Euplotes crassus Tec1 and Tec2 elements: Identification of putative transposase coding regions // Gene. 1993. V. 133. № 1. P. 71–78. https://doi.org/10.1016/0378-1119(93)90226-s
  17. Chen X., Landweber L.F. Phylogenomic analysis reveals genome-wide purifying selection on TBE transposons in the ciliate Oxytricha // Mob. DNA. 2016. V. 7. № 2. https://doi.org/10.1186/s13100-016-0057-9
  18. Dupeyron M., Singh K.S., Bass C., Hayward A. Evolution of Mutator transposable elements across eukaryotic diversity // Mob. DNA. 2019. V. 10. № 12. https://doi.org/10.1186/s13100-019-0153-8
  19. Doak T.G., Witherspoon D.J., Jahn C.L., Herrick G. Selection on the genes of Euplotes crassus Tec1 and Tec2 transposons: Evolutionary appearance of a programmed frameshift in a Tec2 gene encoding a tyrosine family site-specific recombinase // Eukaryot. Cell. 2003. V. 2. № 1. P. 95–102. https://doi.org/10.1128/EC.2.1.95-102.2003
  20. Altschul S.F., Madden T.L., Schäffer A.A. et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs // Nucl. Ac. Res. 1997. V. 25. № 17. P. 3389–3402. https://doi.org/10.1093/nar/25.17.3389
  21. Buchan D.W.A., Jones D.T. The PSIPRED protein analysis workbench: 20 years on // Nucl. Ac. Res. 2019. V. 47. P. 402–407. https://doi.org/10.1093/nar/gkz297
  22. Crooks G.E., Hon G., Chandonia J.M., Brenner S.E. WebLogo: A sequence logo generator // Genome Res. 2004. V. 14. № 6. P. 1188–1190. https://doi.org/10.1101/gr.849004
  23. Hoang D.T., Chernomor O., von Haeseler A. et al. UFBoot2: Improving the ultrafast bootstrap approximation // Mol. Biol. Evol. 2018. V. 35. № 2. P. 518–522. https://doi.org/10.1093/molbev/msx281
  24. Kalyaanamoorthy S., Minh B.Q., Wong T.K.F. et al. ModelFinder: Fast model selection for accurate phylogenetic estimates // Nat. Methods. 2017. V. 14. № 6. P. 587–589. https://doi.org/10.1038/nmeth.4285
  25. Yamada K.D., Tomii K., Katoh K. Application of the MAFFT sequence alignment program to large data – Reexamination of the usefulness of chained guide trees // Bioinformatics. V. 32. № 21. P. 3246–3251. https://doi.org/10.1093/bioinformatics/btw4122016
  26. Kumar M., Suleski J.E., Craig A.E. et al. TimeTree 5: An expanded resource for species divergence times // Mol. Biol. Evol. 2022. V. 39(8). https://doi.org/10.1093/molbev/msac174
  27. Wallau G. L., Ortiz M. F., Loreto E. L. Horizontal transposon transfer in eukarya: detection, bias, and perspectives // Genome Biol. Evol. 2012. V. 4. № 8. P. 689–699. https://doi.org/10.1093/gbe/evs055
  28. Melo E.S., Wallau G.L. Mosquito genomes are frequently invaded by transposable elements through horizontal transfer // PLoS Genet. 2020. V. 16(11). https://doi.org/10.1371/journal.pgen.1008946
  29. Blumenstiel J.P. Birth, school, work, death, and resurrection: The life stages and dynamics of transposable element proliferation // Genes (Basel). 2019. V. 10. № 5. https://doi.org/10.3390/genes10050336

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2. Fig. 1. The structure of transposons of the superfamily L31. 1 tpn–1000 pn; KIP/SIP – terminal inverted repeats or sub-terminal inverted repeats; OPC – an open reading frame encoding a transposase; OPC2 – an open reading frame encoding a protein with an unknown function.

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3. Fig. 2. Phylogenetic diversity of L31 transposons. A graphical representation of the generalized sequences of the fragment of the region of the second aspartate of the catalytic domain of the transposase of six-ray corals is indicated to the right of the dendrogram. Bootstrap values of less than 50% are not indicated on the dendrogram.

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4. Fig. 3. Multiple alignment of L31 transposase sequences-transposons of six-ray corals. The names of potentially functional elements are indicated in bold italics. The α-helices of the DNA-binding domain are highlighted in gray. The intended NLS is indicated in bold italics. The DDE triad of the catalytic domain is shown in black. The GPRK motif is indicated in bold and underlined.

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