Replication and Active Partition of Integrative and Conjugative Elements (ICEs) of the SXT/R391 Family: The Line between ICEs and Conjugative Plasmids Is Getting Thinner

PLoS Genetics

Volumn 11, Issue 6, 2015, Pages

  Carraro, Nicolas ^a   Poulin, Dominique ^a   Burrus, Vincent ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIUM CONJUGATION; CELL DIVISION; GENE DELETION; GENE DOSAGE; GENE LOCUS; GENE LOSS; GENE REPLICATION; GENE TRANSFER; GENETIC STABILITY; HIPAB GENE; MOLECULAR GENETICS; NONHUMAN; ORIT GENE; PLASMID; PROTEIN FAMILY; PROVIDENCIA RETTGERI; R391 INTEGRATIVE AND CONJUGATIVE ELEMENT; SRPMRC GENE; TRAG GENE; TRAI GENE; ANTIBIOTIC RESISTANCE; DNA REPLICATION; GAMMAPROTEOBACTERIA; GENETICS; MULTIGENE FAMILY; R FACTOR; TRANSPOSON;

GAMMAPROTEOBACTERIA; PROVIDENCIA RETTGERI; VIBRIO CHOLERAE;

TRANSPOSON;

CONJUGATION, GENETIC; DNA REPLICATION; DNA TRANSPOSABLE ELEMENTS; DRUG RESISTANCE, BACTERIAL; GAMMAPROTEOBACTERIA; GENES, BACTERIAL; MULTIGENE FAMILY; R FACTORS;

EID: 84937774473     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005298     Document Type: Article

References (102)

1. Guglielmini J, Quintais L, Garcillan-Barcia MP, de la Cruz F, Rocha EP, The Repertoire of ICE in Prokaryotes Underscores the Unity, Diversity, and Ubiquity of Conjugation. PLoS Genet. 2011;7(8):e1002222. Epub 2011/08/31. doi: 10.1371/journal.pgen.1002222 21876676
2. Ghinet MG, Bordeleau E, Beaudin J, Brzezinski R, Roy S, Burrus V, Uncovering the prevalence and diversity of integrating conjugative elements in actinobacteria. PLoS One. 2011;6(11):e27846. Epub 2011/11/25. doi: 10.1371/journal.pone.0027846 22114709
3. Bordeleau E, Ghinet MG, Burrus V, Diversity of integrating conjugative elements in actinobacteria: Coexistence of two mechanistically different DNA-translocation systems. Mob Genet Elements. 2012;2(2):119–24. Epub 2012/08/31. 22934248
4. Wozniak RA, Waldor MK, Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol. 2010;8(8):552–63. Epub 2010/07/06. doi: 10.1038/nrmicro2382 20601965
5. Burrus V, Waldor MK, Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol. 2004;155(5):376–86. Epub 2004/06/23. 15207870
6. Burrus V, Pavlovic G, Decaris B, Guedon G, Conjugative transposons: the tip of the iceberg. Mol Microbiol. 2002;46(3):601–10. Epub 2002/11/02. 12410819
7. Carraro N, Burrus V, Biology of Three ICE Families: SXT/R391, ICEBs1, and ICESt1/ICESt3. Microbiology Spectrum. 2014;2(6). doi: 10.1128/microbiolspec.PLAS-0010-2013 25705574
8. de la Cruz F, Frost LS, Meyer RJ, Zechner EL, Conjugative DNA metabolism in Gram-negative bacteria. FEMS Microbiol Rev. 2010;34(1):18–40. Epub 2009/11/19. doi: 10.1111/j.1574-6976.2009.00195.x 19919603
9. Burrus V, Marrero J, Waldor MK, The current ICE age: biology and evolution of SXT-related integrating conjugative elements. Plasmid. 2006;55(3):173–83. Epub 2006/03/15. 16530834
10. Wozniak RA, Fouts DE, Spagnoletti M, Colombo MM, Ceccarelli D, Garriss G, et al. Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet. 2009;5(12):e1000786. Epub 2009/12/31. doi: 10.1371/journal.pgen.1000786 20041216
11. Spagnoletti M, Ceccarelli D, Rieux A, Fondi M, Taviani E, Fani R, et al. Acquisition and evolution of SXT-R391 integrative conjugative elements in the seventh-pandemic Vibrio cholerae lineage. MBio. 2014;5(4). Epub 2014/08/21.
12. Waldor MK, Tschape H, Mekalanos JJ, A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J Bacteriol. 1996;178(14):4157–65. Epub 1996/07/01. 8763944
13. Boltner D, MacMahon C, Pembroke JT, Strike P, Osborn AM, R391: a conjugative integrating mosaic comprised of phage, plasmid, and transposon elements. J Bacteriol. 2002;184(18):5158–69. 12193633
14. Poulin-Laprade D, Matteau D, Jacques PE, Rodrigue S, Burrus V, Transfer activation of SXT/R391 integrative and conjugative elements: unraveling the SetCD regulon. Nucleic Acids Res. 2015;in press. Epub 2015/02/11.
15. Beaber JW, Hochhut B, Waldor MK, SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature. 2004;427(6969):72–4. Epub 2003/12/23. 14688795
16. Burrus V, Waldor MK, Formation of SXT tandem arrays and SXT-R391 hybrids. J Bacteriol. 2004;186(9):2636–45. 15090504
17. Hochhut B, Beaber JW, Woodgate R, Waldor MK, Formation of chromosomal tandem arrays of the SXT element and R391, two conjugative chromosomally integrating elements that share an attachment site. J Bacteriol. 2001;183(4):1124–32. 11157923
18. Garriss G, Waldor MK, Burrus V, Mobile antibiotic resistance encoding elements promote their own diversity. PLoS Genet. 2009;5(12):e1000775. doi: 10.1371/journal.pgen.1000775 20019796
19. Pembroke JT, Murphy DB, Isolation and analysis of a circular form of the IncJ conjugative transposon-like elements, R391 and R997: implications for IncJ incompatibility. FEMS Microbiol Lett. 2000;187(2):133–8. Epub 2000/06/17. 10856646
20. Carraro N, Libante V, Morel C, Decaris B, Charron-Bourgoin F, Leblond P, et al. Differential regulation of two closely related integrative and conjugative elements from Streptococcus thermophilus. BMC Microbiol. 2011;11:238. Epub 2011/10/26. doi: 10.1186/1471-2180-11-238 22024428
21. Dimopoulou ID, Russell JE, Mohd-Zain Z, Herbert R, Crook DW, Site-specific recombination with the chromosomal tRNA(Leu) gene by the large conjugative Haemophilus resistance plasmid. Antimicrob Agents Chemother. 2002;46(5):1602–3. Epub 2002/04/18. 11959612
22. Grohmann E, Autonomous plasmid-like replication of Bacillus ICEBs1: a general feature of integrative conjugative elements? Mol Microbiol. 2010;75(2):261–3. Epub 2009/12/01. doi: 10.1111/j.1365-2958.2009.06978.x 19943906
23. Kiewitz C, Larbig K, Klockgether J, Weinel C, Tummler B, Monitoring genome evolution ex vivo: reversible chromosomal integration of a 106 kb plasmid at two tRNA(Lys) gene loci in sequential Pseudomonas aeruginosa airway isolates. Microbiology. 2000;146 (Pt 10):2365–73. 11021913
24. Lee CA, Babic A, Grossman AD, Autonomous plasmid-like replication of a conjugative transposon. Mol Microbiol. 2010;75(2):268–79. Epub 2009/12/01. doi: 10.1111/j.1365-2958.2009.06985.x 19943900
25. Sitkiewicz I, Green NM, Guo N, Mereghetti L, Musser JM, Lateral gene transfer of streptococcal ICE element RD2 (region of difference 2) encoding secreted proteins. BMC Microbiol. 2011;11:65. Epub 2011/04/05. doi: 10.1186/1471-2180-11-65 21457552
26. Burrus V, Waldor MK, Control of SXT integration and excision. J Bacteriol. 2003;185(17):5045–54. 12923077
27. Kobayashi I, Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res. 2001;29(18):3742–56. Epub 2001/09/15. 11557807
28. Bahl MI, Hansen LH, Sorensen SJ, Persistence mechanisms of conjugative plasmids. Methods Mol Biol. 2009;532:73–102. Epub 2009/03/10. doi: 10.1007/978-1-60327-853-9_5 19271180
29. Van Melderen L, Saavedra De Bast M, Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet. 2009;5(3):e1000437. Epub 2009/03/28. doi: 10.1371/journal.pgen.1000437 19325885
30. Van Melderen L, Toxin-antitoxin systems: why so many, what for? Curr Opin Microbiol. 2010;13(6):781–5. Epub 2010/11/03. doi: 10.1016/j.mib.2010.10.006 21041110
31. Hayes F, Van Melderen L, Toxins-antitoxins: diversity, evolution and function. Crit Rev Biochem Mol Biol. 2011;46(5):386–408. Epub 2011/08/09. doi: 10.3109/10409238.2011.600437 21819231
32. Wozniak RA, Waldor MK, A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet. 2009;5(3):e1000439. Epub 2009/03/28. doi: 10.1371/journal.pgen.1000439 19325886
33. Dziewit L, Jazurek M, Drewniak L, Baj J, Bartosik D, The SXT conjugative element and linear prophage N15 encode toxin-antitoxin-stabilizing systems homologous to the tad-ata module of the Paracoccus aminophilus plasmid pAMI2. J Bacteriol. 2007;189(5):1983–97. Epub 2006/12/13. 17158670
34. Schumacher MA, Piro KM, Xu W, Hansen S, Lewis K, Brennan RG, Molecular mechanisms of HipA-mediated multidrug tolerance and its neutralization by HipB. Science. 2009;323(5912):396–401. Epub 2009/01/20. doi: 10.1126/science.1163806 19150849
35. Hansen S, Vulic M, Min J, Yen TJ, Schumacher MA, Brennan RG, et al. Regulation of the Escherichia coli HipBA toxin-antitoxin system by proteolysis. PLoS One. 2012;7(6):e39185. Epub 2012/06/22. doi: 10.1371/journal.pone.0039185 22720069
36. Bahl MI, Hansen LH, Sorensen SJ, Impact of conjugal transfer on the stability of IncP-1 plasmid pKJK5 in bacterial populations. FEMS Microbiol Lett. 2007;266(2):250–6. Epub 2006/11/30. 17132149
37. Beaber JW, Hochhut B, Waldor MK, Genomic and functional analyses of SXT, an integrating antibiotic resistance gene transfer element derived from Vibrio cholerae. J Bacteriol. 2002;184(15):4259–69. Epub 2002/07/11. 12107144
38. Ceccarelli D, Daccord A, Rene M, Burrus V, Identification of the origin of transfer (oriT) and a new gene required for mobilization of the SXT/R391 family of integrating conjugative elements. J Bacteriol. 2008;190(15):5328–38. Epub 2008/06/10. doi: 10.1128/JB.00150-08 18539733
39. Marchler-Bauer A, Bryant SH, CD-Search: protein domain annotations on the fly. Nucleic Acids Res. 2004;32(Web Server issue):W327–31. Epub 2004/06/25. 15215404
40. Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, et al. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res. 2013;41(Database issue):D348–52. Epub 2012/12/01. doi: 10.1093/nar/gks1243 23197659
41. Kelley LA, Sternberg MJ, Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc. 2009;4(3):363–71. Epub 2009/02/28. doi: 10.1038/nprot.2009.2 19247286
42. Salje J, Gayathri P, Lowe J, The ParMRC system: molecular mechanisms of plasmid segregation by actin-like filaments. Nat Rev Microbiol. 2010;8(10):683–92. Epub 2010/09/17. doi: 10.1038/nrmicro2425 20844556
43. Moller-Jensen J, Borch J, Dam M, Jensen RB, Roepstorff P, Gerdes K, Bacterial mitosis: ParM of plasmid R1 moves plasmid DNA by an actin-like insertional polymerization mechanism. Mol Cell. 2003;12(6):1477–87. Epub 2003/12/24. 14690601
44. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37(Web Server issue):W202–8. Epub 2009/05/22. doi: 10.1093/nar/gkp335 19458158
45. Schumacher MA, Bacterial plasmid partition machinery: a minimalist approach to survival. Curr Opin Struct Biol. 2012;22(1):72–9. Epub 2011/12/14. doi: 10.1016/j.sbi.2011.11.001 22153351
46. Nonaka L, Maruyama F, Miyamoto M, Miyakoshi M, Kurokawa K, Masuda M, Novel conjugative transferable multiple drug resistance plasmid pAQU1 from Photobacterium damselae subsp. damselae isolated from marine aquaculture environment. Microbes Environ. 2012;27(3):263–72. Epub 2012/03/27. 22446310
47. Johnson TJ, Lang KS, IncA/C plasmids: An emerging threat to human and animal health? Mob Genet Elements. 2012;2(1):55–8. Epub 2012/07/04. 22754754
48. Carraro N, Sauve M, Matteau D, Lauzon G, Rodrigue S, Burrus V, Development of pVCR94DeltaX from Vibrio cholerae, a prototype for studying multidrug resistant IncA/C conjugative plasmids. Front Microbiol. 2014;5:44. Epub 2014/02/26. doi: 10.3389/fmicb.2014.00044 24567731
49. Murata T, Ohnishi M, Ara T, Kaneko J, Han CG, Li YF, et al. Complete nucleotide sequence of plasmid Rts1: implications for evolution of large plasmid genomes. J Bacteriol. 2002;184(12):3194–202. Epub 2002/05/25. 12029035
50. Maeda K, Nojiri H, Shintani M, Yoshida T, Habe H, Omori T, Complete nucleotide sequence of carbazole/dioxin-degrading plasmid pCAR1 in Pseudomonas resinovorans strain CA10 indicates its mosaicity and the presence of large catabolic transposon Tn4676. J Mol Biol. 2003;326(1):21–33. 12547188
51. Yano H, Miyakoshi M, Ohshima K, Tabata M, Nagata Y, Hattori M, et al. Complete nucleotide sequence of TOL plasmid pDK1 provides evidence for evolutionary history of IncP-7 catabolic plasmids. J Bacteriol. 2010;192(17):4337–47. Epub 2010/06/29. doi: 10.1128/JB.00359-10 20581207
52. Jensen RB, Gerdes K, Partitioning of plasmid R1. The ParM protein exhibits ATPase activity and interacts with the centromere-like ParR-parC complex. J Mol Biol. 1997;269(4):505–13. Epub 1997/06/20. 9217256
53. Moller-Jensen J, Ringgaard S, Mercogliano CP, Gerdes K, Lowe J, Structural analysis of the ParR/parC plasmid partition complex. EMBO J. 2007;26(20):4413–22. Epub 2007/09/28. 17898804
54. Lawley TD, Taylor DE, Characterization of the double-partitioning modules of R27: correlating plasmid stability with plasmid localization. J Bacteriol. 2003;185(10):3060–7. Epub 2003/05/06. 12730165
55. Le SQ, Gascuel O, An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25(7):1307–20. Epub 2008/03/28. doi: 10.1093/molbev/msn067 18367465
56. Novick RP, Clowes RC, Cohen SN, Curtiss R, 3rdDatta N, Falkow S, Uniform nomenclature for bacterial plasmids: a proposal. Bacteriol Rev. 1976;40(1):168–89. Epub 1976/03/01. 1267736
57. Wellington EM, Boxall AB, Cross P, Feil EJ, Gaze WH, Hawkey PM, et al. The role of the natural environment in the emergence of antibiotic resistance in gram-negative bacteria. Lancet Infect Dis. 2013;13(2):155–65. Epub 2013/01/26. doi: 10.1016/S1473-3099(12)70317-1 23347633
58. Hawkey PM, The growing burden of antimicrobial resistance. J Antimicrob Chemother. 2008;62 Suppl 1:i1–9. Epub 2008/08/14. doi: 10.1093/jac/dkn241 18684701
59. Auchtung JM, Lee CA, Monson RE, Lehman AP, Grossman AD, Regulation of a Bacillus subtilis mobile genetic element by intercellular signaling and the global DNA damage response. Proc Natl Acad Sci U S A. 2005;102(35):12554–9. Epub 2005/08/18. 16105942
60. Burrus V, Quezada-Calvillo R, Marrero J, Waldor MK, SXT-related integrating conjugative element in New World Vibrio cholerae. Appl Environ Microbiol. 2006;72(4):3054–7. Epub 2006/04/07. 16598018
61. McCool JD, Long E, Petrosino JF, Sandler HA, Rosenberg SM, Sandler SJ, Measurement of SOS expression in individual Escherichia coli K-12 cells using fluorescence microscopy. Mol Microbiol. 2004;53(5):1343–57. Epub 2004/09/25. 15387814
62. Bahl MI, Hansen LH, Licht TR, Sorensen SJ, Conjugative transfer facilitates stable maintenance of IncP-1 plasmid pKJK5 in Escherichia coli cells colonizing the gastrointestinal tract of the germfree rat. Appl Environ Microbiol. 2007;73(1):341–3. Epub 2006/11/07. 17085707
63. Llosa M, Gomis-Ruth FX, Coll M, de la Cruz Fd F, Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol. 2002;45(1):1–8. Epub 2002/07/09. 12100543
64. Qiu X, Gurkar AU, Lory S, Interstrain transfer of the large pathogenicity island (PAPI-1) of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 2006;103(52):19830–5. Epub 2006/12/21. 17179047
65. Juhas M, Power PM, Harding RM, Ferguson DJ, Dimopoulou ID, Elamin AR, et al. Sequence and functional analyses of Haemophilus spp. genomic islands. Genome Biol. 2007;8(11):R237. Epub 2007/11/13. 17996041
66. Klockgether J, Reva O, Larbig K, Tummler B, Sequence analysis of the mobile genome island pKLC102 of Pseudomonas aeruginosa C. J Bacteriol. 2004;186(2):518–34. Epub 2004/01/02. 14702321
67. Mohd-Zain Z, Turner SL, Cerdeno-Tarraga AM, Lilley AK, Inzana TJ, Duncan AJ, et al. Transferable antibiotic resistance elements in Haemophilus influenzae share a common evolutionary origin with a diverse family of syntenic genomic islands. J Bacteriol. 2004;186(23):8114–22. Epub 2004/11/18. 15547285
68. Ryan MP, Pembroke JT, Adley CC, Novel Tn4371-ICE like element in Ralstonia pickettii and genome mining for comparative elements. BMC Microbiol. 2009;9:242. Epub 2009/11/28. doi: 10.1186/1471-2180-9-242 19941653
69. She Q, Phan H, Garrett RA, Albers SV, Stedman KM, Zillig W, Genetic profile of pNOB8 from Sulfolobus: the first conjugative plasmid from an archaeon. Extremophiles. 1998;2(4):417–25. Epub 1998/11/25. 9827331
70. Surtees JA, Funnell BE, Plasmid and chromosome traffic control: how ParA and ParB drive partition. Curr Top Dev Biol. 2003;56:145–80. Epub 2003/10/31. 14584729
71. She Q, Brugger K, Chen L, Archaeal integrative genetic elements and their impact on genome evolution. Res Microbiol. 2002;153(6):325–32. Epub 2002/09/18. 12234006
72. She Q, Shen B, Chen L, Archaeal integrases and mechanisms of gene capture. Biochem Soc Trans. 2004;32(Pt 2):222–6. Epub 2004/03/30. 15046576
73. Marenda M, Barbe V, Gourgues G, Mangenot S, Sagne E, Citti C, A new integrative conjugative element occurs in Mycoplasma agalactiae as chromosomal and free circular forms. J Bacteriol. 2006;188(11):4137–41. Epub 2006/05/19. 16707706
74. Miyakoshi M, Shintani M, Inoue K, Terabayashi T, Sai F, Ohkuma M, et al. ParI, an orphan ParA family protein from Pseudomonas putida KT2440-specific genomic island, interferes with the partition system of IncP-7 plasmids. Environ Microbiol. 2012;14(11):2946–59. Epub 2012/08/29. doi: 10.1111/j.1462-2920.2012.02861.x 22925377
75. Baek JH, Rajagopala SV, Chattoraj DK, Chromosome segregation proteins of Vibrio cholerae as transcription regulators. MBio. 2014;5(3):e01061–14. Epub 2014/05/08. doi: 10.1128/mBio.01061-14 24803519
76. Yurimoto H, Hirai R, Matsuno N, Yasueda H, Kato N, Sakai Y, HxlR, a member of the DUF24 protein family, is a DNA-binding protein that acts as a positive regulator of the formaldehyde-inducible hxlAB operon in Bacillus subtilis. Mol Microbiol. 2005;57(2):511–9. Epub 2005/06/28. 15978081
77. Toussaint A, Merlin C, Mobile elements as a combination of functional modules. Plasmid. 2002;47(1):26–35. Epub 2002/01/19. 11798283
78. Bose B, Auchtung JM, Lee CA, Grossman AD, A conserved anti-repressor controls horizontal gene transfer by proteolysis. Mol Microbiol. 2008;70(3):570–82. Epub 2008/09/03. doi: 10.1111/j.1365-2958.2008.06414.x 18761623
79. Bose B, Grossman AD, Regulation of horizontal gene transfer in Bacillus subtilis by activation of a conserved site-specific protease. J Bacteriol. 2011;193(1):22–9. Epub 2010/11/03. doi: 10.1128/JB.01143-10 21036995
80. Audette GF, Manchak J, Beatty P, Klimke WA, Frost LS, Entry exclusion in F-like plasmids requires intact TraG in the donor that recognizes its cognate TraS in the recipient. Microbiology. 2007;153(Pt 2):442–51. Epub 2007/01/30. 17259615
81. Marrero J, Waldor MK, Determinants of entry exclusion within Eex and TraG are cytoplasmic. J Bacteriol. 2007;189(17):6469–73. Epub 2007/06/19. 17573467
82. Carraro N, Matteau D, Luo P, Rodrigue S, Burrus V, The master activator of IncA/C conjugative plasmids stimulates genomic islands and multidrug resistance dissemination. PLoS Genet. 2014;10(10):e1004714. Epub 2014/10/24. doi: 10.1371/journal.pgen.1004714 25340549
83. Carraro N, Matteau D, Burrus V, Rodrigue S, Unraveling the regulatory network of IncA/C plasmid mobilization: when genomic islands hijack conjugative elements. Mob Genet Elements. 2015;in press.
84. Bousquet A, Henquet S, Compain F, Genel N, Arlet G, Decre D, Partition locus-based classification of selected plasmids in Klebsiella pneumoniae, Escherichia coli and Salmonella enterica spp.: An additional tool. J Microbiol Methods. 2015. Epub 2015/01/28.
85. Harmer CJ, Hall RM, The A to Z of A/C plasmids. Plasmid. 2015. Epub 2015/04/26.
86. McGrath BM, O'Halloran JA, Pembroke JT, Pre-exposure to UV irradiation increases the transfer frequency of the IncJ conjugative transposon-like elements R391, R392, R705, R706, R997 and pMERPH and is recA+ dependent. FEMS Microbiol Lett. 2005;243(2):461–5. Epub 2005/02/03. 15686850
87. Beaber JW, Burrus V, Hochhut B, Waldor MK, Comparison of SXT and R391, two conjugative integrating elements: definition of a genetic backbone for the mobilization of resistance determinants. Cell Mol Life Sci. 2002;59(12):2065–70. Epub 2003/02/06. 12568332
88. Hochhut B, Waldor MK, Site-specific integration of the conjugal Vibrio cholerae SXT element into prfC. Mol Microbiol. 1999;32(1):99–110. Epub 1999/04/27. 10216863
89. McGrath BM, Pembroke JT, Detailed analysis of the insertion site of the mobile elements R997, pMERPH, R392, R705 and R391 in E. coli K12. FEMS Microbiol Lett. 2004;237(1):19–26. Epub 2004/07/23. 15268933
90. Murphy DB, Pembroke JT, Monitoring of chromosomal insertions of the IncJ elements R391 and R997 in Escherichia coli K-12. FEMS Microbiol Lett. 1999;174(2):355–61. 10339829
91. Datta S, Costantino N, Court DL, A set of recombineering plasmids for gram-negative bacteria. Gene. 2006;379:109–15. Epub 2006/06/06. 16750601
92. Datsenko KA, Wanner BL, One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A. 2000;97(12):6640–5. Epub 2000/06/01. doi: 10.1073/pnas.120163297 10829079
93. Haldimann A, Wanner BL, Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J Bacteriol. 2001;183(21):6384–93. Epub 2001/10/10. 11591683
94. Dower WJ, Miller JF, Ragsdale CW, High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res. 1988;16(13):6127–45. 3041370
95. Thomason LC, Costantino N, Court DL, E. coli genome manipulation by P1 transduction. Curr Protoc Mol Biol. 2007;Chapter 1:Unit 1 17. Epub 2008/02/12. doi: 10.1002/0471142727.mb0117s79 18265391
96. Cherepanov PP, Wackernagel W, Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene. 1995;158(1):9–14. Epub 1995/05/26. 7789817
97. Sanchez A, Rech J, Gasc C, Bouet JY, Insight into centromere-binding properties of ParB proteins: a secondary binding motif is essential for bacterial genome maintenance. Nucleic Acids Res. 2013;41(5):3094–103. Epub 2013/01/25. doi: 10.1093/nar/gkt018 23345617
98. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9. Epub 2013/10/18. doi: 10.1093/molbev/mst197 24132122
99. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402. Epub 1997/09/01. 9254694
100. Edgar RC, MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7. Epub 2004/03/23. 15034147
101. Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T, trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–3. Epub 2009/06/10. doi: 10.1093/bioinformatics/btp348 19505945
102. Letunic I, Bork P, Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res. 2011;39(Web Server issue):W475–8. Epub 2011/04/08. doi: 10.1093/nar/gkr201 21470960