Abstract
Mobile genetic elements (MGEs) have a significant impact on genome structure and function being also a source of new genes. As a result of “molecular domestication,” genes encoded by MGEs become functional parts of the host genome. The IS630/Tc1/mariner (ITm) DNA transposon superfamily is one of the most widespread and diverse. To date, several genes are known to have resulted from the ITm transposon co-option. The aim of the present work was to search for the ctenophore Mnemiopsis leidyi genes with integrated fragments of ITm-transposons and subsequent analysis of their of expression levels. In the present work, the local alignment method (BLASTn) was used to search for the hypothetical chimeric genes. The analysis of differential gene activity was performed with the combined use of the Kallisto and Sleuth software. No cDNAs were found that would match the full coding sequence of any M. leidyi ITm transposase. However, 21 unique transcripts of hypothetical chimeric genes containing regions homologous to ITm transposons have been found. Transcriptional analysis showed that during early embryonic development, as well as in the crest and epithelium tissues of adult animals, most hypothetical chimeric genes are not expressed or are expressed at a low level. However, several loci showed differential activity levels during regeneration. The differential activity of some hypothetical chimeric genes during regeneration may indicate their possible “domestication” and involvement in molecular genetic processes in ctenophores.
REFERENCES
Sinzelle, L., Izsvák, Z., and Ivics, Z., Molecular domestication of transposable elements: from detrimental parasites to useful host genes, Cell. Mol. Life Sci., 2009, vol. 66, no. 6, pp. 1073–1093. https://doi.org/10.1007/s00018-009-8376-3
Bourque, G., Burns, K.H., Gehring, M., Gorbunova, V., Seluanov, A., Mager, D.L., and Feschotte, C., Ten things you should know about transposable elements, Genome Biol., 2018, vol. 19 p. 199. https://doi.org/10.1186/s13059-018-1577-z
Yurchenko, N.N., Kovalenko, L.V., and Zakharov, I.K., Transposable elements: Instability of genes and genomes. Russ. J. Genet.: Appl. Res., 2011, vol. 1, no. 6, pp. 489–496. https://doi.org/10.1134/S2079059711060141
Piacentini, L., Fanti, L., Specchia, V., Bozzetti, M.P., Berloco, M., Palumbo, G., and Pimpinelli, S., Transposons, environmental changes, and heritable induced phenotypic variability, Chromosoma, 2014, vol. 123, no. 4, pp. 345–354. https://doi.org/10.1007/s00412-014-0464-y
Auvinet, J., Graça, P., Belkadi, L., Petit, L., Bonnivard, E., Dettaï, A., et al., Mobilization of retrotransposons as a cause of chromosomal diversification and rapid speciation: The case for the Antarctic teleost genus Trematomus, BMC Genomics, 2018, vol. 19, no. 1, p. 339. https://doi.org/10.1186/s12864-018-4714-x
Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J.L., Capy, P., Chalhoub, B., et al., A unified classification system for eukaryotic transposable elements, Nat. Rev. Genet., 2007, vol. 8, no. 12, pp. 973–982. https://doi.org/10.1038/nrg2165
Kojima, K.K., Human transposable elements in Repbase: Genomic footprints from fish to humans, Mobile DNA, 2018, vol. 9, p. 2. https://doi.org/10.1186/s13100-017-0107-y
Yuan, Y.W. and Wessler, S.R., The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, no. 19, pp. 7884–7889. https://doi.org/10.1073/pnas.1104208108
Dupeyron, M., Baril, T., Bass, C., and Hayward, A., Phylogenetic analysis of the Tc1/mariner superfamily reveals the unexplored diversity of pogo-like elements, Mobile DNA, 2020, vol. 11, p. 21. https://doi.org/10.1186/s13100-020-00212-0
Gao, B., Wang, Y., Diaby, M., Zong, W., Shen, D., Wang, S., et al., Evolution of pogo, a separate superfamily of IS630-Tc1-mariner transposons, revealing recurrent domestication events in vertebrates, Mobile DNA, 2020, vol. 11, p. 25. https://doi.org/10.1186/s13100-020-00220-0
Shao, H. and Tu, Z., Expanding the diversity of the IS630-Tc1-mariner superfamily: Discovery of a unique DD37E transposon and reclassification of the DD37D and DD39D transposons, Genetics, 2001, vol. 159, no. 3, pp. 1103–1115. https://doi.org/10.1093/genetics/159.3.1103
Tellier, M., Bouuaert, C.C., and Chalmers, R., Mariner and the ITm superfamily of transposons, Microbiol. Spectrum, 2015, vol. 3, no. 2, p. MDNA3-0033-2014. https://doi.org/10.1128/microbiolspec.MDNA3-0033-2014
Zhang, H.H., Shen, Y.H., Xiong, X.M., Han, M.J., and Zhang, X.G., Identification and evolutionary history of the DD41D transposons in insects, Genes Genomics, 2016, vol. 38, pp. 109–117. https://doi.org/10.1007/s13258-015-0356-4
Shen, D., Gao, B., Miskey, C., Chen, C., Sang, Y., Zong, W., et al., Multiple invasions of visitor, a DD41D family of Tc1/mariner transposons, throughout the evolution of vertebrates, Genome Biol. Evol., 2020, vol. 12, no. 7, pp. 1060–1073. https://doi.org/10.1093/gbe/evaa135
Wang, S., Diaby, M., Puzakov, M., Ullah, N., Wang, Y., Danley, P., et al., Divergent evolution profiles of DD37D and DD39D families of Tc1/mariner transposons in eukaryotes, Mol. Phylogenet. Evol., 2021, vol. 161 p. 107143. https://doi.org/10.1016/j.ympev.2021.107143
Feschotte, C. and Pritham, E.J., DNA transposons and the evolution of eukaryotic genomes, Annu. Rev. Genet., 2007, vol. 41, pp. 331–368. https://doi.org/10.1146/annurev.genet.40.110405.090448
Liu, Y. and Yang, G., Tc1-like transposable elements in plant genomes, Mobile DNA, 2014, vol. 5, p. 17. PMID 24926322; PMCID PMC4054914. https://doi.org/10.1186/1759-8753-5-1724926322
Emmons, S.W., Yesner, L., Ruan, K.S., and Katzenberg, D., Evidence for a transposon in Caenorhabditis elegans, Cell, 1983, vol. 32, no. 1, pp. 55–65. https://doi.org/10.1016/0092-8674(83)90496-8
Franz, G. and Savakis, C., Minos, a new transposable element from Drosophila hydei, is a member of the Tc1-like family of transposons, Nucleic Acids Res., 1991, vol. 19, no. 23, p. 6646. https://doi.org/10.1093/nar/19.23.6646
Langin, T., Capy, P., and Daboussi, M.J., The transposable element Impala, a fungal member of the Tc1-mariner superfamily, Mol. Gen. Genet., 1995, vol. 246, no. 1, pp. 19–28. https://doi.org/10.1007/BF00290129
Schaack, S., Gilbert, C., and Feschotte, C., Promiscuous DNA: Horizontal transfer of transposable elements and why it matters for eukaryotic evolution, Trends Ecol. Evol., 2010, vol. 25, no. 9, pp. 537–546. https://doi.org/10.1016/j.tree.2010.06.001
Puzakov, M.V., Puzakova, L.V., Cheresiz, S.V., and Sang, Y., The IS630/Tc1/mariner transposons in three ctenophore genomes, Mol. Phylogenet. Evol., 2021, vol. 163, p. 107231. https://doi.org/10.1016/j.ympev.2021.107231
Bowen, N.J. and Jordan, I.K., Exaptation of protein coding sequences from transposable elements, Genome Dyn., 2007, vol. 3, pp. 147–162. https://doi.org/10.1159/000107609
Jangam, D., Feschotte, C., and Betrán, E., Transposable element domestication as an adaptation to evolutionary conflicts, Trends Genet., 2017, vol. 33, no. 11, pp. 817–831. https://doi.org/10.1016/j.tig.2017.07.011
Kapitonov, V.V. and Jurka, J., RAG1 core and V (D) J recombination signal sequences were derived from Transib transposons, PLoS Biol., 2005, vol. 3, no. 6, p. e181. https://doi.org/10.1371/journal.pbio.0030181
Panchin, Y. and Moroz, L.L., Molluscan mobile elements similar to the vertebrate recombination-activating genes, Biochem. Biophys. Res. Commun., 2008, vol. 369, no. 3, pp. 818–823. https://doi.org/10.1016/j.bbrc.2008.02.097
Kim, H.S., Chen, Q., Kim, S.K., Nickoloff, J.A., Hromas, R., Georgiadis, M.M., and Lee, S.H., The DDN catalytic motif is required for Metnase functions in non-homologous end joining (NHEJ) repair and replication restart, J. Biol. Chem., 2014, vol. 289, no. 15, pp. 10930–10938. https://doi.org/10.1074/jbc.M113.533216
Mateo, L., Ullastres, A., and González, J., A transposable element insertion confers xenobiotic resistance in Drosophila, PLoS Genet., 2014, vol. 10, no. 8, p. e1004560. https://doi.org/10.1371/journal.pgen.1004560
Mills, C.E., 1998-Present. Phylum Ctenophora: List of All Valid Species Names. https://faculty.washington.edu/cemills/Ctenolist.html. Accessed March 30, 2017.
Pang, K. and Martindale, M.Q., Developmental expression of homeobox genes in the ctenophore Mnemiopsis leidyi, Dev. Genes Evol., 2008, vol. 218, pp. 307–319. https://doi.org/10.1007/s00427-008-0222-3
Moroz, L.L., Kocot, K.M., Citarella, M.R., Dosung, S., Norekian, T.P., Povolotskaya, I.S., et al., The ctenophore genome and the evolutionary origins of neural systems, Nature, 2014, vol. 10, no. 7503, pp. 109–114. https://doi.org/10.1038/nature13400
Ryan, J.F., Pang, K., Schnitzler, C.E., Nguyen, A.D., Moreland, R.T., Simmons, D.K., Koch, B.J., Francis, W.R., Havlak, P., Comparative Sequencing Program N.I.S.C., Smith, S.A., Putnam, N.H., Haddock, S.H., Dunn, C.W., Wolfsberg, T.G., Mullikin, J.C., Martindale, M.Q., and Baxevanis, A.D., The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution, Science, 2013, vol. 342, no. 6164, p. 1242592. https://doi.org/10.1126/science.1242592
Jekely, G., Paps, J., and Nielsen, C., The phylogenetic position of ctenophores and the origin(s) of nervous systems, Evodevo, 2015, vol. 6, pp. 1–8. https://doi.org/10.1186/2041-9139-6-1
Vinogradov, M.E., Shushkina, E.A., Musaeva, E.I., and Sorokin, P.Yu., A newly acclimated species in the Black Sea: The ctenophore Mnemiopsis leidyi (Ctenophora: Lobata), Oceanology, 1989, vol. 29, no. 2, pp. 220–224.
Shiganova, T.A., Ctenophore Mnemiopsis leidyi and ichthyoplankton in the Sea of Marmara in October 1992, Oceanology, 1993, vol. 33, no. 6, pp. 900–903.
Ivanov, V.P., Kamakin, A.M., and Ushivtzev, V.B., Invasion of the Caspian Sea by the comb jellyfish Mnemiopsis leidyi (Ctenophora), Biol. Invasions, 2000, vol. 2, pp. 255–258. https://doi.org/10.1023/A:1010098624728
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res., 1997, vol. 25, pp. 3389–3402. https://doi.org/10.1093/nar/25.17.3389
Wheeler, D.L., Barrett, T., Benson, D.A., Bryant, S.H., Canese, K., Chetvernin, V., et al., Database resources of the National Center for Biotechnology Information, Nucleic Acids Res., 2008, vol. 36, no. 1, pp. 13–21. https://doi.org/10.1093/nar/gkm1000
Bray, N.L., Pimentel, H., Melsted, P., and Pachter, L., Near-optimal probabilistic RNA-seq quantification, Nat. Biotechnol., 2016, vol. 34, no. 5, pp. 525–527. https://doi.org/10.1038/nbt.3519
Pimentel, H., Bray, N.L., Puente, S., Melsted, P., and Pachter, L., Differential analysis of RNA-seq incorporating quantification uncertainty, Nat. Methods, 2017, vol. 14, no. 7, pp. 687–690. https://doi.org/10.1038/nmeth.4324
Funding
This work was supported by the “Functional, Metabolic, and Toxicological Aspects of Hydrobionts and Their Populations in Biotopes with Different Physical and Chemical Conditions” state order to the Kovalevsky Institute of the Biology of Southern Seas (state registration no. 121041400077-1) and the Russian Foundation for Basic Research and the city of Sevastopol (project no. 18-44-920002).
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Puzakov, M.V., Puzakova, L.V. & Ulupova, Y.N. Differential Activity of Genes with IS630/TC1/MARINER Transposon Fragments in the Genome of the Ctenophore Mnemiopsis leidyi. Mol. Genet. Microbiol. Virol. 37, 194–201 (2022). https://doi.org/10.3103/S089141682204005X
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DOI: https://doi.org/10.3103/S089141682204005X