Structure and evolution of DNA transposons of the L31 superfamily of bivalves

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Abstract

DNA transposons of the IS630/Tc1/mariner (ITm) are widespread representatives of DNA transposons that make a significant contribution to the evolution of eukaryotic genomes. With the start of large-scale application of next generation sequencing (NGS) technologies and the emergence of many new whole genome sequences of organisms in nucleotide collections, ITm elements have been identified in most taxa of the eukaryotic tree of life. Despite the rather detailed study of the diversity of ITm representatives, elements are still found that contribute to the expansion and revision of the classification of this group of DNA transposons. This paper presents for the first time a detailed analysis of the L31 elements of bivalves, which resulted in a description of the structure, diversity, distribution, and phylogenetic position among the ITm elements. It was found that L31 transposons are an independent superfamily in the ITm group, which has an ancient origin. Within the L31 clade, rather high diversity was observed: five phylogenetic clusters were identified. At the moment, the presence of L31 transposons in molluscs has been revealed only in bivalves in the subclass Autobranchia, with a predominance in diversity and quantity in the infraclass Pteriomorphia. It has also been shown that the protein encoded by the second open reading frame (ORF2) is an integral structural component of almost all full-length L31 elements. The data obtained contribute to a better understanding of the evolution of representatives of ITm transposons. Further study of L31 transposons in other taxa (cnidaria), as well as the study of the function of the second ORF protein, will provide an opportunity to better understand the evolution of DNA transposons, the mechanisms of horizontal transfer, and the contribution to eukaryotic biodiversity.

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M. V. Puzakov

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

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

L. V. Puzakova

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

Email: puzakov@ngs.ru
Russian Federation, Sevastopol, 299011

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2. Fig. 1. Structure of transposes of the Tc1/mariner and pogo superfamilies (a) and diversity of the structure of L31 elements of bivalves (b). TIR/SIP – terminal inverted repeats or subterminal inverted repeats; ORF – open reading frame encoding transposase; ORF2 is an open reading frame encoding a protein of unknown function.

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3. Fig. 2. Phylogenetic diversity of L31 elements of bivalves. The names of the clades are indicated to the right of the dendrogram. Geometric figures denote the transposons identified in this study: square – order Ostreida, circle – order Mytilida, diamond – order Pectinida, triangle with its apex up – orders Adapedonta and Venerida, triangle with its apex down – order Pterioida. Bootstrap values less than 50% are not shown on the dendrogram.

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4. Fig. 3. Distribution of L31 transposons among bivalves. nd – no data; a slash separates the number of species in which L31 elements were found and the total number of studied species of the taxon; *in some species only short fragments (scraps) of L31 elements were identified (see text and Table 2). The taxonomic tree was created using data from the World Register of Marine Species (WoRMS) (https://www.marinespecies.org/) and TimeTree (http://www.timetree.org/).

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5. Fig. 4. Multiple alignment of L31 transposon transposase sequences. The α-helices of the DNA binding domain are highlighted in gray. The proposed NLS is indicated in bold italic. The DDE triad of the catalytic domain is highlighted in black. The GPRK motif is shown in bold and underlined.

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6. Fig. 5. Features of conserved regions of the catalytic domain of transposase elements L31. Marker amino acid residues of the catalytic domain are highlighted in gray.

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