title: Self-synthesizing transposons: unexpected key players in the evolution of viruses and defense systems.
abstract: Self-synthesizing transposons are the largest known transposable elements that encode their own DNA polymerases (DNAP). The Polinton/Maverick family of self-synthesizing transposons is widespread in eukaryotes and abundant in the genomes of some protists. In addition to the DNAP and a retrovirus-like integrase, most of the polintons encode homologs of the major and minor jelly-roll capsid proteins, DNA-packaging ATPase and capsid maturation protease. Therefore, polintons are predicted to alternate between the transposon and viral lifestyles although virion formation remains to be demonstrated. Polintons are related to a group of eukaryotic viruses known as virophages that parasitize on giant viruses of the family Mimiviridae and another recently identified putative family of polinton-like viruses (PLV) predicted to lead a similar, dual life style. Comparative genomic analysis of polintons, virophages, PLV and the other viruses with double-stranded (ds)DNA genomes infecting eukaryotes and prokaryotes suggests that the polintons evolved from bacterial tectiviruses and could have been the ancestors of a broad range of eukaryotic viruses including adenoviruses and members of the proposed order 'Megavirales' as well as linear cytoplasmic plasmids. Recently, a group of predicted self-synthesizing transposons was discovered also in prokaryotes. These elements, denoted casposons, encode a DNAP and a homolog of the CRISPR-associated Cas1 endonuclease that has an integrase activity but no capsid proteins. Thus, unlike polintons, casposons appear to be limited to the transposon life style although they could have evolved from viruses. The casposons are thought to have played a pivotal role in the origin of the prokaryotic adaptive immunity, giving rise to the adaptation module of the CRISPR-Cas systems.
authors.affiliation: Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Department of Microbiology, Institut Pasteur, Paris, France. Electronic address: krupovic@pasteur.fr.
authors.forename: Mart
authors.initials: M
authors.lastname: Krupovic
authors.affiliation: National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. Electronic address: koonin@ncbi.nlm.nih.gov.
authors.forename: Eugene V
authors.initials: EV
authors.lastname: Koonin
mesh_terms: D064130:CRISPR-Associated Proteins / Q000235:genetics*; D064113:CRISPR-Cas Systems / Q000235:genetics; D004251:DNA Transposable Elements / Q000235:genetics*; D004279:DNA, Viral / Q000096:biosynthesis / Q000235:genetics; D004259:DNA-Directed DNA Polymerase / Q000235:genetics; D056890:Eukaryota / Q000235:genetics / Q000821:virology*; D056686:Mimiviridae / Q000235:genetics*; D011387:Prokaryotic Cells / Q000821:virology*; D000071819:Virophages / Q000235:genetics*
chemical_list: D064130:CRISPR-Associated Proteins; D004251:DNA Transposable Elements; D004279:DNA, Viral; D004259:DNA-Directed DNA Polymerase
references.citation: Proc Natl Acad Sci U S A. 2011 Apr 12;108(15):6163-8
references.pmid: 21444812
references.citation: Front Microbiol. 2014 Jul 21;5:354
references.pmid: 25101062
references.citation: J Gen Virol. 2003 Nov;84(Pt 11):2895-908
references.pmid: 14573794
references.citation: Virology. 2015 May;479-480:2-25
references.pmid: 25771806
references.citation: J Virol. 2015 Jan 15;89(2):1278-85
references.pmid: 25392206
references.citation: Nat Rev Microbiol. 2015 Nov;13(11):722-36
references.pmid: 26411297
references.citation: Front Microbiol. 2015 Nov 27;6:1308
references.pmid: 26640459
references.citation: Ann N Y Acad Sci. 2015 Apr;1341:10-24
references.pmid: 25727355
references.citation: Proc Natl Acad Sci U S A. 2012 Nov 6;109(45):18431-6
references.pmid: 23091035
references.citation: Gene. 2007 Apr 1;390(1-2):3-17
references.pmid: 17034960
references.citation: Science. 2009 May 15;324(5929):935-8
references.pmid: 19372392
references.citation: Nat Struct Mol Biol. 2014 Jun;21(6):528-34
references.pmid: 24793649
references.citation: Proc Natl Acad Sci U S A. 2012 Oct 30;109(44):18078-83
references.pmid: 23071316
references.citation: Nat Rev Microbiol. 2014 Jul;12(7):479-92
references.pmid: 24909109
references.citation: Ann N Y Acad Sci. 2009 Oct;1178:276-84
references.pmid: 19845643
references.citation: Nucleic Acids Res. 2015 Dec 15;43(22):10576-87
references.pmid: 26573596
references.citation: Biol Direct. 2011 Jul 14;6:38
references.pmid: 21756346
references.citation: Ann N Y Acad Sci. 2015 Apr;1341:106-14
references.pmid: 25581723
references.citation: Curr Opin Virol. 2011 Aug;1(2):118-24
references.pmid: 22440622
references.citation: Virol J. 2013 May 23;10:158
references.pmid: 23701946
references.citation: Virology. 2014 Aug;462-463:107-14
references.pmid: 24971703
references.citation: Nucleic Acids Res. 2002 Jun 1;30(11):2524-37
references.pmid: 12034842
references.citation: Proc Natl Acad Sci U S A. 2015 Sep 22;112(38):E5318-26
references.pmid: 26305943
references.citation: PLoS Biol. 2005 Jun;3(6):e181
references.pmid: 15898832
references.citation: Biol Direct. 2006 Mar 16;1:7
references.pmid: 16545108
references.citation: Biol Direct. 2015 Apr 25;10:19
references.pmid: 25909276
references.citation: Curr Opin Virol. 2014 Apr;5:105-10
references.pmid: 24747680
references.citation: Genome Dyn. 2012;7:1-28
references.pmid: 22759811
references.citation: Nat Rev Microbiol. 2015 Feb;13(2):105-15
references.pmid: 25534808
references.citation: Virol J. 2014 May 14;11:95
references.pmid: 24886672
references.citation: Proc Natl Acad Sci U S A. 2006 Mar 21;103(12):4540-5
references.pmid: 16537396
references.citation: Proc Natl Acad Sci U S A. 2015 Sep 22;112(38):11750-1
references.pmid: 26330604
references.citation: Nat Rev Microbiol. 2008 Dec;6(12):941-8
references.pmid: 19008892
references.citation: Science. 2011 Apr 8;332(6026):231-4
references.pmid: 21385722
references.citation: Nat Rev Genet. 2015 Mar;16(3):184-92
references.pmid: 25488578
references.citation: Mob DNA. 2014 Aug 26;5:23
references.pmid: 25180049
references.citation: Mob DNA. 2010 Jan 25;1(1):3
references.pmid: 20226081
references.citation: Nucleic Acids Res. 2011 Oct;39(19):8291-305
references.pmid: 21742758
references.citation: Proc Natl Acad Sci U S A. 2010 Nov 9;107(45):19508-13
references.pmid: 20974979
references.citation: Genomics Inform. 2014 Sep;12(3):87-97
references.pmid: 25317107
references.citation: J Virol. 2013 Apr;87(8):4225-36
references.pmid: 23408616
references.citation: Nature. 2015 Mar 12;519(7542):193-8
references.pmid: 25707795
references.citation: Elife. 2015 Aug 18;4:null
references.pmid: 26284603
references.citation: Nature. 2008 Sep 4;455(7209):100-4
references.pmid: 18690211
references.citation: Genome Biol Evol. 2016 Jan 13;8(2):375-86
references.pmid: 26764427
references.citation: Annu Rev Genet. 2009;43:49-66
references.pmid: 19653859
references.citation: Sci Rep. 2014 Jun 18;4:5347
references.pmid: 24939392
references.citation: Virol J. 2013 Apr 04;10:106
references.pmid: 23557328
references.citation: Arch Virol. 2013 Dec;158(12):2517-21
references.pmid: 23812617
references.citation: Biol Direct. 2015 Apr 28;10:20
references.pmid: 25928409
references.citation: Trends Genet. 2005 Oct;21(10):551-2
references.pmid: 16084623
references.citation: PLoS One. 2014 Apr 18;9(4):e94923
references.pmid: 24747414
references.citation: BMC Biol. 2015 Nov 11;13:95
references.pmid: 26560305
references.citation: BMC Biol. 2014 May 19;12:36
references.pmid: 24884953
references.citation: Proc Natl Acad Sci U S A. 2013 Jun 25;110(26):10800-5
references.pmid: 23754393
references.citation: Arch Virol. 2016 Jan;161(1):233-47
references.pmid: 26446887
references.citation: Curr Opin Virol. 2013 Oct;3(5):578-86
references.pmid: 23850154
references.citation: Adv Virus Res. 2012;82:63-89
references.pmid: 22420851
references.citation: Biol Direct. 2014 Apr 29;9:6
references.pmid: 24773695