Horizontal transfer of transposons between and within crustaceans and insects

BackgroundHorizontal transfer of transposable elements (HTT) is increasingly appreciated as an important source of genome and species evolution in eukaryotes. However, our understanding of HTT dynamics is still poor in eukaryotes because the diversity of species for which whole genome sequences are available is biased and does not reflect the global eukaryote diversity.ResultsIn this study we characterized two Mariner transposable elements (TEs) in the genome of several terrestrial crustacean isopods, a group of animals particularly underrepresented in genome databases. The two elements have a patchy distribution in the arthropod tree and they are highly similar (>93% over the entire length of the element) to insect TEs (Diptera and Hymenoptera), some of which were previously described in Ceratitis rosa (Crmar2) and Drosophila biarmipes (Mariner-5_Dbi). In addition, phylogenetic analyses and comparisons of TE versus orthologous gene distances at various phylogenetic levels revealed that the taxonomic distribution of the two elements is incompatible with vertical inheritance.ConclusionsWe conclude that the two Mariner TEs each underwent at least three HTT events. Both elements were transferred once between isopod crustaceans and insects and at least once between isopod crustacean species. Crmar2 was also transferred between tephritid and drosophilid flies and Mariner-5 underwent HT between hymenopterans and dipterans. We demonstrate that these various HTTs took place recently (most likely within the last 3 million years), and propose iridoviruses and/or Wolbachia endosymbionts as potential vectors of these transfers.

[1]  Thomas Walker,et al.  Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti , 2009, BMC Genomics.

[2]  C. Feschotte,et al.  A role for host–parasite interactions in the horizontal transfer of transposons across phyla , 2010, Nature.

[3]  J. Shultz,et al.  Pancrustacean phylogeny: hexapods are terrestrial crustaceans and maxillopods are not monophyletic , 2005, Proceedings of the Royal Society B: Biological Sciences.

[4]  Y. Bigot,et al.  Species sympatry and horizontal transfers of Mariner transposons in marine crustacean genomes. , 2006, Molecular phylogenetics and evolution.

[5]  R. Cordaux,et al.  The impact of endosymbionts on the evolution of host sex-determination mechanisms. , 2011, Trends in genetics : TIG.

[6]  P. Capy,et al.  Automatic classification within families of transposable elements: application to the mariner Family. , 2009, Gene.

[7]  X. Maside,et al.  The ant genomes have been invaded by several types of mariner transposable elements , 2012, Naturwissenschaften.

[8]  Joel Dudley,et al.  TimeTree: a public knowledge-base of divergence times among organisms , 2006, Bioinform..

[9]  Ramón Doallo,et al.  CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics , 2012, Nature Methods.

[10]  Sudhir Kumar,et al.  Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks. , 2003, Molecular biology and evolution.

[11]  H. Robertson Evolution of DNA Transposons in Eukaryotes , 2002 .

[12]  N. Okada,et al.  Poxviruses as possible vectors for horizontal transfer of retroposons from reptiles to mammals , 2007, Proceedings of the National Academy of Sciences.

[13]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[14]  P. Capy,et al.  A New Basal Subfamily of mariner Elements in Ceratitis rosa and Other Tephritid Flies , 2001, Journal of Molecular Evolution.

[15]  A. van Dorsselaer,et al.  The glycosylated androgenic hormone of the terrestrial isopod Porcellio scaber (Crustacea). , 2004, General and comparative endocrinology.

[16]  J. Palmer,et al.  Horizontal gene transfer in eukaryotic evolution , 2008, Nature Reviews Genetics.

[17]  Alan M. Lambowitz,et al.  Mobile DNA III , 2002 .

[18]  C. Cruaud,et al.  Complete genome sequence of invertebrate iridescent virus 22 isolated from a blackfly larva. , 2013, The Journal of general virology.

[19]  R. Plasterk,et al.  Resident aliens: the Tc1/mariner superfamily of transposable elements. , 1999, Trends in genetics : TIG.

[20]  J. Jurka Repbase update: a database and an electronic journal of repetitive elements. , 2000, Trends in genetics : TIG.

[21]  M. F. Ortiz,et al.  Horizontal Transposon Transfer in Eukarya: Detection, Bias, and Perspectives , 2012, Genome biology and evolution.

[22]  John E. Johnson,et al.  Host RNAs, including transposons, are encapsidated by a eukaryotic single-stranded RNA virus , 2012, Proceedings of the National Academy of Sciences.

[23]  Jonathan B. Clark,et al.  Factors that affect the horizontal transfer of transposable elements. , 2004, Current issues in molecular biology.

[24]  M. Houck,et al.  Possible horizontal transfer of Drosophila genes by the mite Proctolaelaps regalis , 1991, Science.

[25]  Marian Thomson,et al.  Analysis of the genome sequences of three Drosophila melanogaster spontaneous mutation accumulation lines. , 2009, Genome research.

[26]  D. Adelson,et al.  Jumping the fine LINE between species: Horizontal transfer of transposable elements in animals catalyses genome evolution , 2013, BioEssays : news and reviews in molecular, cellular and developmental biology.

[27]  T. Williams Natural invertebrate hosts of iridoviruses (Iridoviridae). , 2008, Neotropical entomology.

[28]  P. Broly,et al.  The origin of terrestrial isopods (Crustacea: Isopoda: Oniscidea) , 2013, Evolutionary Ecology.

[29]  S. Beatson,et al.  Draft genome sequence of the male-killing Wolbachia strain wBol1 reveals recent horizontal gene transfers from diverse sources , 2013, BMC Genomics.

[30]  H. Backhaus,et al.  TCl4.7: a novel lepidopteran transposon found in Cydia pomonella granulosis virus. , 1995, Virology.

[31]  Molecular subgrouping of Wolbachia and bacteriophage WO infection among some Indian Drosophila species , 2011, Journal of Genetics.

[32]  R. Cordaux,et al.  Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission , 2001 .

[33]  A. Rambaut,et al.  Estimating Divergence Dates and Substitution Rates in the Drosophila Phylogeny , 2012, Molecular biology and evolution.

[34]  M. G. Kidwell Voyage of an ancient mariner , 1993, Nature.

[35]  J. Shultz,et al.  Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences , 2010, Nature.

[36]  J. Bennetzen,et al.  A unified classification system for eukaryotic transposable elements , 2007, Nature Reviews Genetics.

[37]  A. Cutter Divergence times in Caenorhabditis and Drosophila inferred from direct estimates of the neutral mutation rate. , 2008, Molecular biology and evolution.

[38]  Cédric Feschotte,et al.  Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. , 2010, Trends in ecology & evolution.

[39]  M. Woolfit,et al.  An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. , 2009, Molecular biology and evolution.

[40]  Z. Tu,et al.  Possible horizontal transfer of a transposable element from host to parasitoid. , 2001, Molecular biology and evolution.

[41]  C. Marino,et al.  Wolbachia in Anastrepha Fruit Flies (Diptera: Tephritidae) , 2009, Current Microbiology.

[42]  M. Sharkey Phylogeny and Classification of Hymenoptera , 2007 .

[43]  George E. Davis,et al.  An Updated Classification Of The Recent Crustacea , 2001 .

[44]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[45]  Hugh M. Robertson,et al.  The mariner transposable element is widespread in insects , 1993, Nature.

[46]  D. Bouchon,et al.  Phylogenetic analysis of mitochondrial LSU rRNA in oniscids. , 2000, Comptes rendus de l'Academie des sciences. Serie III, Sciences de la vie.

[47]  J. DeWoody,et al.  Hosts, parasites, and horizontal gene transfer. , 2013, Trends in parasitology.

[48]  J. Vlak,et al.  Horizontal Escape of the Novel Tc1-Like Lepidopteran Transposon TCp3.2 into Cydia pomonella Granulovirus , 1998, Journal of Molecular Evolution.

[49]  M. Quail,et al.  Phylogenetic Relationships of the Wolbachia of Nematodes and Arthropods , 2006, PLoS pathogens.

[50]  Maxim Teslenko,et al.  MrBayes 3.2: Efficient Bayesian Phylogenetic Inference and Model Choice Across a Large Model Space , 2012, Systematic biology.

[51]  R. Cordaux,et al.  Feminizing / Wolbachia/ and the evolution of sex determination in isopods , 2008 .

[52]  D. Witherspoon,et al.  Recent horizontal transfer of mellifera subfamily mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. , 2003, Molecular biology and evolution.

[53]  D. Hartl,et al.  Modern thoughts on an ancyent marinere: function, evolution, regulation. , 1997, Annual review of genetics.

[54]  Todd H. Oakley,et al.  The Ecoresponsive Genome of Daphnia pulex , 2011, Science.

[55]  A. Meyer,et al.  Horizontal Transfers of Tc1 Elements between Teleost Fishes and Their Vertebrate Parasites, Lampreys , 2012, Genome biology and evolution.

[56]  E. Paccagnini,et al.  Iridovirus infection in terrestrial isopods from Sicily (Italy). , 2013, Tissue & cell.