The diversity of prokaryotic DDE transposases of the mutator superfamily, insertion specificity, and association with conjugation machineries

Genome Biology and Evolution

Volumn 6, Issue 2, 2014, Pages 260-272

  Guérillot, Romain ^a,b,c   Siguier, Patricia ^b   Gourbeyre, Edith ^b   Chandler, Michael ^b   Glaser, Philippe ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

Evolution; Genome dynamics; Insertion sequence; Integrative and conjugative element; Transposase

Indexed keywords

BACTERIAL PROTEIN; TRANSPOSASE; TRANSPOSON;

AMINO ACID SEQUENCE; BACTERIA; BACTERIUM CONJUGATION; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MULTIGENE FAMILY; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; SEQUENCE ALIGNMENT; TRANSPOSON;

AMINO ACID SEQUENCE; BACTERIA; BACTERIAL PROTEINS; CONJUGATION, GENETIC; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; TRANSPOSASES;

EID: 84902952147     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evu010     Document Type: Article

References (55)

1. Altschul SF, et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Amyotte SG, et al. 2012. Transposable elements in phytopathogenic Verticillium spp.: insights into genome evolution and inter- and intra- specific diversification. BMC Genomics 13: 314.
3. Aziz RK, Breitbart M, Edwards RA. 2010. Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res. 38: 4207-4217.
4. Barsoum E, Martinez P, Astrom SU. 2010. Alpha3, a transposable element that promotes host sexual reproduction. Genes Dev. 24: 33-44.
5. Bennetzen JL. 1984. Transposable elementMu1 is found in multiple copies only in Robertson's Mutator maize lines. J Mol Appl Genet. 2: 519-524.
6. Berger B, Haas D. 2001. Transposase and cointegrase: specialized transposition proteins of the bacterial insertion sequence IS21 and related elements. Cell Mol Life Sci. 58: 403-419.
7. Bhadra R, et al. 2006. Cascade PSI-BLAST web server: a remote homology search tool for relating protein domains. Nucleic Acids Res. 34: W143-W146. (Pubitemid 44529752)
8. Brochet M, Couve E, Glaser P, Guedon G, Payot S. 2008. Integrative conjugative elements and related elements are major contributors to the genome diversity of Streptococcus agalactiae. J Bacteriol. 190: 6913-6917.
9. Brochet M, et al. 2009. Atypical association of DDE transposition with conjugation specifies a new family of mobile elements. Mol Microbiol. 71: 948-959.
10. Calcutt MJ, Lewis MS, Wise KS. 2002. Molecular genetic analysis of ICEF, an integrative conjugal element that is present as a repetitive sequence in the chromosome of Mycoplasma fermentans PG18. J Bacteriol. 184: 6929-6941.
11. Chandler M, Fayet O. 1993. Translational frameshifting in the control of transposition in bacteria. Mol Microbiol. 7: 497-503.
12. Cline MS, et al. 2007. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc. 2: 2366-2382.
13. Cole C, Barber JD, Barton GJ. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36:W197-W201.
14. Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res. 14: 1188-1190.
15. Curcio MJ, Derbyshire KM. 2003. The outs and ins of transposition: from Mu to kangaroo. Nat Rev Mol Cell Biol. 4: 865-877.
16. Darriba D, Taboada GL, Doallo R, Posada D. 2011. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164-1165.
17. Dordet Frisoni E, et al. 2013. ICEA of Mycoplasma agalactiae: a new family of self-transmissible integrative elements that confers conjugative properties to the recipient strain. Mol Microbiol. 89: 1226-1239.
18. Eisen JA, Benito MI,Walbot V. 1994. Sequence similarity of putative transposases links the maize Mutator autonomous element and a group of bacterial insertion sequences. Nucleic Acids Res. 22: 2634-2636.
19. Endoh H, Hirayama T, Aoyama T, Oka A. 1990. Characterization of the virA gene of the agropine-type plasmid pRiA4 of Agrobacterium rhizogenes. FEBS Lett. 271: 28-32.
20. Filee J, Siguier P, Chandler M. 2007. Insertion sequence diversity in archaea. Microbiol Mol Biol Rev. 71: 121-157.
21. Guerillot R, Da Cunha V, Sauvage E, Bouchier C, Glaser P. 2013. Modular evolution of TnGBSs, a new family of ICEs associating IS transposition, plasmid replication and conjugation for their spreading. J Bacteriol. 195: 1979-1990.
22. Han X, et al. 2009. Identification of a novel variant of staphylococcal cassette chromosome mec, type II.5, and its truncated form by insertion of putative conjugative transposon Tn6012. Antimicrob Agents Chemother. 53: 2616-2619.
23. Haren L, Ton-Hoang B, Chandler M. 1999. Integrating DNA: transposases and retroviral integrases. Annu Rev Microbiol. 53: 245-281.
24. Hennig S, Ziebuhr W. 2010. Characterization of the transposase encoded by IS256, the prototype of a major family of bacterial insertion sequence elements. J Bacteriol. 192: 4153-4163.
25. Hickman AB, Chandler M, Dyda F. 2010. Integrating prokaryotes and eukaryotes: DNA transposases in light of structure. Crit Rev Biochem Mol Biol. 45: 50-69.
26. Hua-Van A, Capy P. 2008. Analysis of the DDE motif in the Mutator superfamily. J Mol Evol. 67: 670-681.
27. Jiang N, Ferguson AA, Slotkin RK, Lisch D. 2011. Pack-Mutator-like transposable elements (Pack-MULEs) induce directional modification of genes through biased insertion and DNA acquisition. Proc Natl Acad Sci U S A. 108: 1537-1542.
28. Jurka J, et al. 2005. Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 110: 462-467.
29. Kallastu A, Horak R, Kivisaar M. 1998. Identification and characterization of IS1411, a new insertion sequence which causes transcriptional activation of the phenol degradation genes in Pseudomonas putida. J Bacteriol. 180: 5306-5312.
30. Katoh K, Standley DM. 2013. MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability. Mol Biol Evol. 30: 772-780.
31. Kirchner J, Connolly CM, Sandmeyer SB. 1995. Requirement of RNA polymerase III transcription factors for in vitro position-specific integration of a retroviruslike element. Science 267: 1488-1491.
32. Kiss J, Olasz F. 1999. Formation and transposition of the covalently closed IS30 circle: the relation between tandem dimers and monomeric circles. Mol Microbiol. 34: 37-52.
33. Kostriken R, Morita C, Heffron F. 1981. Transposon Tn3 encodes a sitespecific recombination system: identification of essential sequences, genes, and actual site of recombination. Proc Natl Acad Sci U S A. 78: 4041-4045.
34. Loessner I, Dietrich K, Dittrich D, Hacker J, Ziebuhr W. 2002. Transposase-dependent formation of circular IS256 derivatives in Staphylococcus epidermidis and Staphylococcus aureus. J Bacteriol. 184: 4709-4714.
35. Lutkenhaus J. 2012. The ParA/MinD family puts things in their place. Trends Microbiol. 20: 411-418.
36. Mahillon J, Chandler M. 1998. Insertion sequences.Microbiol Mol Biol Rev. 62: 725-774.
37. Marenda M, et al. 2006. A new integrative conjugative element occurs in Mycoplasma agalactiae as chromosomal and free circular forms. J Bacteriol. 188: 4137-4141.
38. Montano SP, Pigli YZ, Rice PA. 2012. The Mu transpososome structure sheds light on DDE recombinase evolution. Nature 491: 413-417.
39. Morris JH, et al. 2011. clusterMaker: a multi-algorithm clustering plugin for Cytoscape. BMC Bioinformatics 12: 436.
40. Nagy Z, Chandler M. 2004. Regulation of transposition in bacteria. Res Microbiol. 155: 387-398.
41. Nagy Z, Szabo M, Chandler M, Olasz F. 2004. Analysis of the N-terminal DNA binding domain of the IS30 transposase. Mol Microbiol. 54: 478-488.
42. Palmer JR, Daniels CJ. 1995. In vivo definition of an archaeal promoter. J Bacteriol. 177: 1844-1849.
43. Polard P, Prere MF, Fayet O, Chandler M. 1992. Transposase-induced excision and circularization of the bacterial insertion sequence IS911. EMBO J. 11: 5079-5090.
44. Rousseau P, Loot C, Turlan C, Nolivos S, Chandler M. 2008. Bias between the left and right inverted repeats during IS911 targeted insertion. J Bacteriol. 190: 6111-6118.
45. Siguier P, Filee J, Chandler M. 2006. Insertion sequences in prokaryotic genomes. Curr Opin Microbiol. 9: 526-531.
46. Siguier P, Gagnevin L, Chandler M. 2009. The new IS1595 family, its relation to IS1 and the frontier between insertion sequences and transposons. Res Microbiol. 160: 232-241.
47. Smyth DS, Robinson DA. 2009. Integrative and sequence characteristics of a novel genetic element, ICE6013, in Staphylococcus aureus. J Bacteriol. 191: 5964-5975.
48. Sundaresan V, Freeling M. 1987. An extrachromosomal form of the Mu transposons of maize. Proc Natl Acad Sci U S A. 84: 4924-4928.
49. Tamura K, et al. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 28: 2731-2739.
50. Thiaucourt F, et al. 2011. Mycoplasma mycoides, from "mycoides Small Colony" to "Capri". A microevolutionary perspective. BMC Genomics 12: 114.
51. Turlan C, Chandler M. 1995. IS1-mediated intramolecular rearrangements: formation of excised transposon circles and replicative deletions. EMBO J. 14: 5410-5421.
52. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 2009. Jalview Version 2 - a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189-1191.
53. Yuan YW, Wessler SR. 2011. The catalytic domain of all eukaryotic cutand- paste transposase superfamilies. Proc Natl Acad Sci U S A. 108: 7884-7889.
54. Ziebuhr W, et al. 1999. A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol. 32: 345-356.
55. Zomer AL, Buist G, Larsen R, Kok J, Kuipers OP. 2007. Time-resolved determination of the CcpA regulon of Lactococcus lactis subsp. cremoris MG1363. J Bacteriol. 189: 1366-1381.