DNA transposons are defined as repeated DNA sequences that can move within the host genome through the action of transposases. The transposon superfamily Merlin was originally found mainly in animal genomes. Here, we describe a global distribution of the Merlin in animals, fungi, plants and protists, reporting for the first time their presence in Rhodophyceae, Metamonada, Discoba and Alveolata. We identified a great variety of potentially active Merlin families, some containing highly imperfect terminal inverted repeats and internal tandem repeats. Merlin-related sequences with no evidence of mobilization capacity were also observed and may be products of domestication. The evolutionary trees support that Merlin is likely an ancient superfamily, with early events of diversification and secondary losses, although repeated re-invasions probably occurred in some groups, which would explain its diversity and discontinuous distribution. We cannot rule out the possibility that the Merlin superfamily is the product of multiple horizontal transfers of related prokaryotic insertion sequences. Moreover, this is the first account of a DNA transposon in kinetoplastid flagellates, with conserved Merlin transposase identified in Bodo saltans and Perkinsela sp., whereas it is absent in trypanosomatids. Based on the level of conservation of the transposase and overlaps of putative open reading frames with Merlin, we propose that in protists it may serve as a raw material for gene emergence.

Faculty of Sciences University of South Bohemia České Budějovice Czech Republic

Institute of Parasitology Biology Center Czech Academy of Sciences České Budějovice Czech Republic

Instituto de Biologia Molecular do Paraná Curitiba PR Brazil

Laboratório de Ciências e Tecnologias Aplicadas em Saúde Curitiba PR Brazil

Pós Graduação em Biologia Celular e Molecular Universidade Federal do Paraná Curitiba PR Brazil

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de Koning APJ, Gu W, Castoe TA, Batzer MA, Pollock DD. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet. 2011;7. 10.1371/journal.pgen.1002384 PubMed DOI PMC

Karakülah G, Suner A. PlanTEnrichment: A tool for enrichment analysis of transposable elements in plants. Genomics. 2017;109: 336–340. 10.1016/j.ygeno.2017.05.008 PubMed DOI

Feschotte C, Jiang N, Wessler SR. Plant transposable elements: where genetics meets genomics. Nat Rev Genet. 2002;3: 329–41. 10.1038/nrg793 PubMed DOI

Kidwell MG, Lisch DR. Perspective: transposable elements, parasitic DNA, and genome evolution. Evolution. 2001;55: 1–24. 10.1111/j.0014-3820.2001.tb01268.x PubMed DOI

Oliver KR, McComb JA, Greene WK. Transposable elements: Powerful contributors to angiosperm evolution and diversity. Genome Biol Evol. 2013;5: 1886–1901. 10.1093/gbe/evt141 PubMed DOI PMC

Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al.. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8: 973–82. 10.1038/nrg2165 PubMed DOI

Han K, Lee J, Meyer TJ, Remedios P, Goodwin L, Batzer MA. L1 recombination-associated deletions generate human genomic variation. Proc Natl Acad Sci U S A. 2008;105: 19366–71. 10.1073/pnas.0807866105 PubMed DOI PMC

Volff J-N. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. BioEssays. 2006;28: 913–22. 10.1002/bies.20452 PubMed DOI

Jangam D, Feschotte C, Betrán E. Transposable element domestication as an adaptation to evolutionary conflicts. Trends Genet. 2017;33: 817–831. 10.1016/j.tig.2017.07.011 PubMed DOI PMC

Schrader L, Schmitz J. The impact of transposable elements in adaptive evolution. Mol Ecol. 2019;28: 1537–1549. 10.1111/mec.14794 PubMed DOI

Finnegan DJ. Eukaryotic transposable elements and genome evolution. Trends Genet. 1989;5: 103–7. 10.1016/0168-9525(89)90039-5 PubMed DOI

Munoz-Lopez M, Garcia-Perez J. DNA transposons: Nature and applications in genomics. Curr Genomics. 2010;11: 115–128. 10.2174/138920210790886871 PubMed DOI PMC

Jurka J, Kapitonov VV-V, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005;110: 462–7. 10.1159/000084979 PubMed DOI

Merlin Feschotte C., a new superfamily of DNA transposons identified in diverse animal genomes and related to bacterial IS1016 insertion sequences. Mol Biol Evol. 2004;21: 1769–80. 10.1093/molbev/msh188 PubMed DOI

Siguier P, Gagnevin L, Chandler M. The new IS1595 family, its relation to IS1 and the frontier between insertion sequences and transposons. Res Microbiol. 2009;160: 232–41. 10.1016/j.resmic.2009.02.003 PubMed DOI

Yuan Y-W, Wessler SR. The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies. Proc Natl Acad Sci U S A. 2011;108: 7884–9. 10.1073/pnas.1104208108 PubMed DOI PMC

Parisot N, Pelin A, Gasc C, Polonais VV, Belkorchia A, Panek J, et al.. Microsporidian genomes harbor a diverse array of transposable elements that demonstrate an ancestry of horizontal exchange with metazoans. Genome Biol Evol. 2014;6: 2289–2300. 10.1093/gbe/evu178 PubMed DOI PMC

Marchler-Bauer A, Bryant SH. CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004;32: W327–31. 10.1093/nar/gkh454 PubMed DOI PMC

Boratyn GM, Camacho C, Cooper PS, Coulouris G, Fong A, Ma N, et al.. BLAST: a more efficient report with usability improvements. Nucleic Acids Res. 2013;41. 10.1093/nar/gkt282 PubMed DOI PMC

Rozewicki J, Li S, Amada KM, Standley DM, Katoh K. MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res. 2019. 10.1093/nar/gkz342 PubMed DOI PMC

Kohany O, Gentles AJ, Hankus L, Jurka J. Annotation, submission and screening of repetitive elements in Repbase: RepbaseSubmitter and Censor. BMC Bioinformatics. 2006;7: 474. 10.1186/1471-2105-7-474 PubMed DOI PMC

Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Battistuzzi FU, editor. Mol Biol Evol. 2018;35: 1547–1549. 10.1093/molbev/msy096 PubMed DOI PMC

Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999;27: 573–80. 10.1093/nar/27.2.573 PubMed DOI PMC

Kelley LA, Sternberg MJE. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc. 2009;4: 363–71. 10.1038/nprot.2009.2 PubMed DOI

Huang Y, Niu B, Gao Y, Fu L, Li W. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics. 2010;26: 680–2. 10.1093/bioinformatics/btq003 PubMed DOI PMC

Pei J, Grishin N-V. PROMALS3D: multiple protein sequence alignment enhanced with evolutionary and three-dimensional structural information. Methods Mol Biol. 2014;1079: 263–71. 10.1007/978-1-62703-646-7_17 PubMed DOI PMC

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25: 1972–3. 10.1093/bioinformatics/btp348 PubMed DOI PMC

Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, et al.. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61: 539–42. 10.1093/sysbio/sys029 PubMed DOI PMC

Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop, GCE. New Orleans, LA; 2010. pp. 1–8. 10.1109/GCE.2010.5676129 DOI

Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30: 1312–3. 10.1093/bioinformatics/btu033 PubMed DOI PMC

Shao H, 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;159: 1103–15. Available: http://www.ncbi.nlm.nih.gov/pubmed/11729156 PubMed PMC

Adl SM, Bass D, Lane CE, Lukeš J, Schoch CL, Smirnov A, et al.. Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot Microbiol. 2019;66: 4–119. 10.1111/jeu.12691 PubMed DOI PMC

Yang Y, Xiong J, Zhou Z, Huo F, Miao W, Ran C, et al.. The genome of the myxosporean Thelohanellus kitauei shows adaptations to nutrient acquisition within its fish host. Genome Biol Evol. 2014;6: 3182–3198. 10.1093/gbe/evu247 PubMed DOI PMC

de Albuquerque NRM, Ebert D, Haag KL. Transposable element abundance correlates with mode of transmission in microsporidian parasites. Mob DNA. 2020;11: 19. 10.1186/s13100-020-00218-8 PubMed DOI PMC

Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, et al.. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 2016;108: 1028–1046. 10.3852/16-042 PubMed DOI PMC

Muszewska A, Steczkiewicz K, Stepniewska-Dziubinska M, Ginalski K. Cut-and-paste transposons in fungi with diverse lifestyles. Genome Biol Evol. 2017;9: 3463–3477. 10.1093/gbe/evx261 PubMed DOI PMC

Glöckner G, Hülsmann N, Schleicher M, Noegel AA, Eichinger L, Gallinger C, et al.. The genome of the foraminiferan Reticulomyxa filosa. Curr Biol. 2014;24: 11–18. 10.1016/j.cub.2013.11.027 PubMed DOI

PPG I. A community-derived classification for extant lycophytes and ferns. J Syst Evol. 2016;54: 563–603. 10.1111/jse.12229 DOI

Cosby RL, Judd J, Zhang R, Zhong A, Garry N, Pritham EJ, et al.. Recurrent evolution of vertebrate transcription factors by transposase capture. Science. 2021;371. 10.1126/science.abc6405 PubMed DOI PMC

Sangiovanni M, Granata I, Thind AS, Guarracino MR. From trash to treasure: detecting unexpected contamination in unmapped NGS data. BMC Bioinformatics. 2019;20: 168. 10.1186/s12859-019-2684-x PubMed DOI PMC

Strong MJ, Xu G, Morici L, Splinter Bon-Durant S, Baddoo M, Lin Z, et al.. Microbial contamination in next generation sequencing: implications for sequence-based analysis of clinical samples. PLoS Pathog. 2014;10: e1004437. 10.1371/journal.ppat.1004437 PubMed DOI PMC

Lusk RW. Diverse and widespread contamination evident in the unmapped depths of high throughput sequencing data. PLoS One. 2014;9: e110808. 10.1371/journal.pone.0110808 PubMed DOI PMC

Francois CM, Durand F, Figuet E, Galtier N. Prevalence and implications of contamination in public genomic resources: a case study of 43 reference arthropod assemblies. G3 (Bethesda). 2020;10: 721–730. 10.1534/g3.119.400758 PubMed DOI PMC

Kissinger JC, DeBarry J. Genome cartography: charting the apicomplexan genome. Trends Parasitol. 2011;27: 345–54. 10.1016/j.pt.2011.03.006 PubMed DOI PMC

Jurka J, Kapitonov V-V, Kohany O, Jurka M-V. Repetitive sequences in complex genomes: structure and evolution. Annu Rev Genomics Hum Genet. 2007;8: 241–59. 10.1146/annurev.genom.8.080706.092416 PubMed DOI

Yan F, Di S, Takahashi R. CACTA-superfamily transposable element is inserted in MYB transcription factor gene of soybean line producing variegated seeds. Genome. 2015;58: 365–74. 10.1139/gen-2015-0054 PubMed DOI

Trubitsyna M, Grey H, Houston DR, Finnegan DJ, Richardson JM. Structural basis for the inverted repeat preferences of mariner transposases. J Biol Chem. 2015;290: 13531–40. 10.1074/jbc.M115.636704 PubMed DOI PMC

Augé-Gouillou C, Hamelin MH, Demattei M V, Periquet M, Bigot Y. The wild-type conformation of the Mos-1 inverted terminal repeats is suboptimal for transposition in bacteria. Mol Genet Genomics. 2001;265: 51–7. 10.1007/s004380000385 PubMed DOI

Naumann TA, Reznikoff WS. Tn5 transposase with an altered specificity for transposon ends. J Bacteriol. 2002;184: 233–40. 10.1128/jb.184.1.233-240.2002 PubMed DOI PMC

d’Avila-Levy CM, Boucinha C, Kostygov A, Santos HLC, Morelli KA, Grybchuk-Ieremenko A, et al.. Exploring the environmental diversity of kinetoplastid flagellates in the high-throughput DNA sequencing era. Mem Inst Oswaldo Cruz. 2015;110: 956–65. 10.1590/0074-02760150253 PubMed DOI PMC

Jackson AP, Otto TD, Aslett M, Armstrong SD, Bringaud F, Schlacht A, et al.. Kinetoplastid phylogenomics reveals the evolutionary innovations associated with the origins of parasitism. Curr Biol. 2016;26: 161–172. 10.1016/j.cub.2015.11.055 PubMed DOI PMC

Tanifuji G, Cenci U, Moog D, Dean S, Nakayama T, David V, et al.. Genome sequencing reveals metabolic and cellular interdependence in an amoeba-kinetoplastid symbiosis. Sci Rep. 2017;7: 11688. 10.1038/s41598-017-11866-x PubMed DOI PMC

Bringaud F, Ghedin E, El-Sayed NM a, Papadopoulou B. Role of transposable elements in trypanosomatids. Microbes Infect. 2008;10: 575–81. 10.1016/j.micinf.2008.02.009 PubMed DOI

El-Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran A-N, et al.. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science. 2005;309: 409–15. 10.1126/science.1112631 PubMed DOI

Peacock CS, Seeger K, Harris D, Murphy L, Ruiz JC, Quail MA, et al.. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat Genet. 2007;39: 839–47. 10.1038/ng2053 PubMed DOI PMC

Butenko A, Hammond M, Field MC, Ginger ML, Yurchenko V, Lukeš J. Reductionist pathways for parasitism in euglenozoans? Expanded datasets provide new insights. Trends Parasitol. 2021;37: 100–116. 10.1016/j.pt.2020.10.001 PubMed DOI

Martínez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K, Myler PJ. Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell. 2003;11: 1291–9. 10.1016/s1097-2765(03)00143-6 PubMed DOI

Campbell DA, Thomas S, Sturm NR. Transcription in kinetoplastid protozoa: why be normal? Microbes Infect. 2003;5: 1231–1240. 10.1016/j.micinf.2003.09.005 PubMed DOI

Ribeiro YC, Robe LJ, Veluza DS, dos Santos CMB, Lopes ALK, Krieger MA, et al.. Study of VIPER and TATE in kinetoplastids and the evolution of tyrosine recombinase retrotransposons. Mob DNA. 2019;10: 34. 10.1186/s13100-019-0175-2 PubMed DOI PMC

Ludwig A, Krieger MA. Genomic and phylogenetic evidence of VIPER retrotransposon domestication in trypanosomatids. Mem Inst Oswaldo Cruz. 2016;111: 765–769. 10.1590/0074-02760160224 PubMed DOI PMC

Smith M, Bringaud F, Papadopoulou B. Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome. BMC Genomics. 2009;10: 240. 10.1186/1471-2164-10-240 PubMed DOI PMC

Arkhipova IR. Using bioinformatic and phylogenetic approaches to classify transposable elements and understand their complex evolutionary histories. Mob DNA. 2017;8: 19. 10.1186/s13100-017-0103-2 PubMed DOI PMC

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. Mob DNA. 2020;11: 25. 10.1186/s13100-020-00220-0 PubMed DOI PMC

Vogt A, Goldman AD, Mochizuki K, Landweber LF. Transposon domestication versus mutualism in ciliate genome rearrangements. PLoS Genet. 2013;9: e1003659. 10.1371/journal.pgen.1003659 PubMed DOI PMC

Inukai T. Role of transposable elements in the propagation of minisatellites in the rice genome. Mol Genet Genomics. 2004;271: 220–7. 10.1007/s00438-003-0973-5 PubMed DOI

Smýkal P, Kalendar R, Ford R, Macas J, Griga M. Evolutionary conserved lineage of Angela-family retrotransposons as a genome-wide microsatellite repeat dispersal agent. Heredity (Edinb). 2009;103: 157–67. 10.1038/hdy.2009.45 PubMed DOI

Paço A, Freitas R, Vieira-da-Silva A. Conversion of DNA Sequences: from a transposable element to a tandem repeat or to a gene. Genes (Basel). 2019;10. 10.3390/genes10121014 PubMed DOI PMC

Belyayev A, Josefiová J, Jandová M, Mahelka V, Krak K, Mandák B. Transposons and satellite DNA: on the origin of the major satellite DNA family in the Chenopodium genome. Mob DNA. 2020;11: 20. 10.1186/s13100-020-00219-7 PubMed DOI PMC

Wilder J, Hollocher H. Mobile elements and the genesis of microsatellites in dipterans. Mol Biol Evol. 2001;18: 384–392. 10.1093/oxfordjournals.molbev.a003814 PubMed DOI

Kapitonov V-V, Holmquist GP, Jurka J. L1 repeat is a basic unit of heterochromatin satellites in cetaceans. Mol Biol Evol. 1998;15: 611–2. 10.1093/oxfordjournals.molbev.a025963 PubMed DOI