title: Horizontal transfer and evolution of prokaryote transposable elements in eukaryotes.
abstract: Horizontal transfer (HT) of transposable elements (TEs) plays a key role in prokaryotic evolution, and mounting evidence suggests that it has also had an important impact on eukaryotic evolution. Although many prokaryote-to-prokaryote and eukaryote-to-eukaryote HTs of TEs have been characterized, only few cases have been reported between prokaryotes and eukaryotes. Here, we carried out a comprehensive search for all major groups of prokaryotic insertion sequences (ISs) in 430 eukaryote genomes. We uncovered a total of 80 sequences, all deriving from the IS607 family, integrated in the genomes of 14 eukaryote species belonging to four distinct phyla (Amoebozoa, Ascomycetes, Basidiomycetes, and Stramenopiles). Given that eukaryote IS607-like sequences are most closely related to cyanobacterial IS607 and that their phylogeny is incongruent with that of their hosts, we conclude that the presence of IS607-like sequences in eukaryotic genomes is the result of several HT events. Selection analyses further suggest that our ability to detect these prokaryote TEs today in eukaryotes is because HT of these sequences occurred recently and/or some IS607 elements were domesticated after HT, giving rise to new eukaryote genes. Supporting the recent age of some of these HTs, we uncovered intact full-length, potentially active IS607 copies in the amoeba Acanthamoeba castellani. Overall, our study shows that prokaryote-to-eukaryote HT of TEs occurred at relatively low frequency during recent eukaryote evolution and it sets IS607 as the most widespread TE (being present in prokaryotes, eukaryotes, and viruses).
authors.affiliation: Université de Poitiers, UMR CNRS 7267 Ecologie et Biologie des Interactions, Equipe Ecologie Evolution Symbiose, Poitiers, France. clement.gilbert@univ-poitiers.fr
authors.forename: Clément
authors.initials: C
authors.lastname: Gilbert
authors.forename: Richard
authors.initials: R
authors.lastname: Cordaux
mesh_terms: D001419:Bacteria / Q000235:genetics; D001483:Base Sequence; D004251:DNA Transposable Elements / Q000235:genetics*; D056890:Eukaryota / Q000235:genetics*; D019143:Evolution, Molecular; D022761:Gene Transfer, Horizontal; D016678:Genome; D010802:Phylogeny; D011387:Prokaryotic Cells
chemical_list: D004251:DNA Transposable Elements
keywords: eukaryotes; horizontal transfer; prokaryotes; transposable elements
references.citation: Proc Natl Acad Sci U S A. 2007 Jul 17;104(29):12046-51
references.pmid: 17623783
references.citation: Genetica. 1999;107(1-3):27-37
references.pmid: 10952195
references.citation: Nature. 2010 Apr 29;464(7293):1347-50
references.pmid: 20428170
references.citation: FEMS Microbiol Rev. 2010 May;34(3):281-94
references.pmid: 20132312
references.citation: Proc Natl Acad Sci U S A. 2009 Sep 22;106(38):16333-8
references.pmid: 19805302
references.citation: Proc Natl Acad Sci U S A. 2012 Feb 7;109(6):1907-12
references.pmid: 22308402
references.citation: Clin Microbiol Infect. 2009 Dec;15 Suppl 2:178-80
references.pmid: 19793120
references.citation: Curr Opin Genet Dev. 2009 Dec;19(6):613-9
references.pmid: 19897356
references.citation: PLoS One. 2009 Jul 02;4(7):e6133
references.pmid: 19582169
references.citation: Theor Appl Genet. 2002 Jan;104(1):48-53
references.pmid: 12579427
references.citation: Nat Rev Microbiol. 2012 Jun 11;10(7):472-82
references.pmid: 22683880
references.citation: Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):942-6
references.pmid: 8302872
references.citation: Front Cell Infect Microbiol. 2012 Aug 21;2:110
references.pmid: 22919697
references.citation: Fungal Genet Biol. 2008 Mar;45(3):266-77
references.pmid: 18039586
references.citation: Mol Biol Evol. 2009 Aug;26(8):1921-9
references.pmid: 19443853
references.citation: Nat Rev Microbiol. 2010 Aug;8(8):552-63
references.pmid: 20601965
references.citation: Science. 2009 Nov 20;326(5956):1112-5
references.pmid: 19965430
references.citation: PLoS One. 2011;6(7):e22780
references.pmid: 21829512
references.citation: Cell Mol Life Sci. 2005 Jun;62(11):1182-97
references.pmid: 15761667
references.citation: Genome Biol Evol. 2010;2:745-56
references.pmid: 20889655
references.citation: Genome Integr. 2010 May 26;1(1):2
references.pmid: 20678256
references.citation: Genetica. 2011 Apr;139(4):489-96
references.pmid: 21451967
references.citation: Annu Rev Genet. 2012;46:341-58
references.pmid: 22934638
references.citation: Bioinformatics. 2010 Oct 1;26(19):2455-7
references.pmid: 20671151
references.citation: Nat Rev Genet. 2009 Oct;10(10):691-703
references.pmid: 19763152
references.citation: Nucleic Acids Res. 1994 Jul 11;22(13):2634-6
references.pmid: 8041625
references.citation: Science. 2006 Sep 1;313(5791):1261-6
references.pmid: 16946064
references.citation: BMC Evol Biol. 2008 Jun 24;8:181
references.pmid: 18577206
references.citation: Biol Direct. 2009 Sep 29;4:34
references.pmid: 19788731
references.citation: Mol Biol Evol. 2012 Sep;29(9):2223-30
references.pmid: 22411854
references.citation: Trends Ecol Evol. 2010 Sep;25(9):537-46
references.pmid: 20591532
references.citation: Proc Natl Acad Sci U S A. 2011 Sep 13;108(37):15258-63
references.pmid: 21878562
references.citation: Genetica. 1999;107(1-3):197-207
references.pmid: 10952213
references.citation: Mol Genet Genomics. 2004 May;271(4):387-93
references.pmid: 15014982
references.citation: Genome Biol Evol. 2012;4(8):689-99
references.pmid: 22798449
references.citation: Curr Opin Microbiol. 2006 Oct;9(5):526-31
references.pmid: 16935554
references.citation: Trends Genet. 2007 Jan;23(1):10-5
references.pmid: 17109990
references.citation: Nat Rev Microbiol. 2005 Sep;3(9):722-32
references.pmid: 16138100
references.citation: Syst Biol. 2003 Oct;52(5):696-704
references.pmid: 14530136
references.citation: Theor Popul Biol. 2010 Dec;78(4):278-88
references.pmid: 20816882
references.citation: Genetics. 2007 Dec;177(4):2293-307
references.pmid: 18073433
references.citation: Mol Genet Genomics. 2008 Nov;280(5):397-408
references.pmid: 18751731
references.citation: Curr Biol. 2009 Jan 27;19(2):R81-8
references.pmid: 19174147
references.citation: PLoS One. 2009 Aug 05;4(8):e6515
references.pmid: 19654869
references.citation: Annu Rev Genet. 2007;41:331-68
references.pmid: 18076328
references.citation: J Bacteriol. 2001 Apr;183(7):2226-33
references.pmid: 11244061
references.citation: Bioinformatics. 2006 Dec 1;22(23):2971-2
references.pmid: 17021158
references.citation: Trends Genet. 2010 Jan;26(1):5-8
references.pmid: 19969385
references.citation: Res Microbiol. 2008 Jun;159(5):325-31
references.pmid: 18572389
references.citation: Bioinformatics. 2011 Apr 15;27(8):1164-5
references.pmid: 21335321
references.citation: Microbiol Mol Biol Rev. 2010 Sep;74(3):434-52
references.pmid: 20805406
references.citation: Mol Biol Evol. 2004 Sep;21(9):1769-80
references.pmid: 15190130
references.citation: Nat Rev Genet. 2008 Aug;9(8):605-18
references.pmid: 18591983
references.citation: Genome Biol Evol. 2011;3:1175-86
references.pmid: 21940637
references.citation: FEMS Yeast Res. 2003 Dec;4(3):233-45
references.pmid: 14654427
references.citation: Nucleic Acids Res. 2012 Jan;40(Database issue):D290-301
references.pmid: 22127870
references.citation: Mol Biol Evol. 2003 Apr;20(4):554-62
references.pmid: 12654937
references.citation: BMC Evol Biol. 2008 Apr 12;8:110
references.pmid: 18405387
references.citation: Nature. 2001 Feb 15;409(6822):860-921
references.pmid: 11237011
references.citation: Eukaryot Cell. 2005 Jun;4(6):1102-15
references.pmid: 15947202
references.citation: PLoS One. 2010 Sep 16;5(9):
references.pmid: 20862282
references.citation: Mol Biol Evol. 2005 Mar;22(3):478-85
references.pmid: 15509724
references.citation: Nature. 2010 Jun 3;465(7298):617-21
references.pmid: 20520714
references.citation: Bioinformatics. 2005 Mar 1;21(5):676-9
references.pmid: 15509596
references.citation: Trends Genet. 2005 Apr;21(4):200-3
references.pmid: 15797612
references.citation: BMC Evol Biol. 2009 Aug 11;9:197
references.pmid: 19664294
references.citation: Mol Biol Evol. 2005 Feb;22(2):308-16
references.pmid: 15483318
references.citation: Mol Biol Evol. 2007 Apr;24(4):969-81
references.pmid: 17251179
references.citation: Philos Trans R Soc Lond B Biol Sci. 2010 Mar 12;365(1541):729-48
references.pmid: 20124341
references.citation: J Bacteriol. 2000 Oct;182(19):5300-8
references.pmid: 10986230
references.citation: Nature. 2000 May 18;405(6784):299-304
references.pmid: 10830951
references.citation: Genome Biol Evol. 2010;2:656-64
references.pmid: 20693155
references.citation: Bioessays. 2009 Jul;31(7):703-14
references.pmid: 19415638
references.citation: Trends Genet. 2011 Apr;27(4):157-63
references.pmid: 21334091