317
Views
2
CrossRef citations to date
0
Altmetric
Review Articles

Integrative Conjugative Elements (ICEs) of the SXT/R391 family drive adaptation and evolution in γ-Proteobacteria

ORCID Icon, ORCID Icon, & ORCID Icon
Pages 105-126 | Received 20 Aug 2022, Accepted 19 Dec 2022, Published online: 12 Jan 2023

References

  • Alvarez-Martinez CE, Christie PJ. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev. 73(4):775–808.
  • Ambrose SJ, Harmer CJ, Hall RM. 2018. Compatibility and entry exclusion of IncA and IncC plasmids revisited: incA and IncC plasmids are compatible. Plasmid. 96–97:7–12.
  • Armshaw P, Pembroke JT. 2013a. Generation and analysis of an ICE R391 deletion library identifies genes involved in the element encoded UV-inducible cell-sensitising function. FEMS Microbiol Lett. 342(1):45–53.
  • Armshaw P, Pembroke JT. 2013b. Control of expression of the ICE R391 encoded UV-inducible cell-sensitising function. BMC Microbiol. 13(1):195.
  • Armshaw P, Pembroke JT. 2015. Examination of the cell sensitizing gene orf43 of ICE R391 suggests a role in ICE transfer enhancement to recipient cells. FEMS Microbiol Lett. 362(4):1–7.
  • Armshaw P, Pembroke JT. 2016. UV stress-responsive genes associated with enterobacterial integrative conjugative elements of the ICE SXT/R391 group. In: Frans J. de Bruijn, editor, Stress and environmental regulation of gene expression and adaptation in bacteria, I&II. Vol. 1. John Wiley & Sons, Inc., Hoboken, New Jersey; p. 517–527.
  • Armshaw P, Piterina AV, Pembroke JT. 2011. Molecular and functional analysis of motility “shut off” in the enteric mobile element R391, an integrative conjugative element from Providencia rettgeri. Proceedings of the Microscopy Society of Ireland Annual Symposium at: CRANN, Trinity College Dublin, Ireland.
  • Baharoglu Z, Bikard D, Mazel D. 2010. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet. 6(10):e1001165.
  • Balado M, Lemos ML, Osorio CR. 2013. Integrating conjugative elements of the SXT/R391 family from fish-isolated Vibrios encode restriction-modification systems that confer resistance to bacteriophages. FEMS Microbiol Ecol. 83(2):457–467.
  • Beaber JW, Burrus V, Hochhut B, Waldor MK. 2002a. Comparison of SXT and R391, two conjugative integrating elements: definition of a genetic backbone for the mobilization of resistance determinants. Cell Mol Life Sci. 59(12):2065–2070.
  • Beaber JW, Hochhut B, Waldor MK. 2002b. Genomic and functional analyses of SXT, an integrating antibiotic resistance gene transfer element derived from Vibrio cholerae. J Bacteriol. 184(15):4259–4269.
  • Beaber JW, Hochhut B, Waldor MK. 2004. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature. 427(6969):72–74.
  • Beaber JW, Waldor MK. 2004. Identification of operators and promoters that control SXT conjugative transfer. J Bacteriol. 186(17):5945–5949.
  • Bednarz M, Halliday JA, Herman C, Golding I. 2014. Revisiting bistability in the lysis/lysogeny circuit of bacteriophage lambda. PLoS One. 9(6):e100876.
  • Bi D, Xu Z, Harrison EM, Tai C, Wei Y, He X, Jia S, Deng Z, Rajakumar K, Ou HY. 2012. ICEberg: a web-based resource for integrative and conjugative elements found in Bacteria. Nucleic Acids Res. 40(Database issue):D621–D626.
  • Bioteau A, Durand R, Burrus V. 2018. Redefinition and unification of the SXT/R391 family of integrative and conjugative elements. Appl Environ Microbiol. 84(13):e00485-18.
  • Böltner D, MacMahon C, Pembroke JT, Strike P, Osborn AM. 2002. R391: a conjugative integrating mosaic comprised of phage, plasmid, and transposon elements. J Bacteriol. 184(18):5158–5169.
  • Bordeleau E, Brouillette E, Robichaud N, Burrus V. 2010. Beyond antibiotic resistance: integrating conjugative elements of the SXT/R391 family that encode novel diguanylate cyclases participate to c-di-gmp signalling in Vibrio cholerae. Environ Microbiol. 12(2):510–523.
  • Botelho J, Schulenburg H. 2021. The role of integrative and conjugative elements in antibiotic resistance evolution. Trends Microbiol. 29(1):8–18.
  • Bradley DE. 1980. Morphological and serological relationships of conjugative pili. Plasmid. 4(2):155–169.
  • Brochet M, Rusniok C, Couvé E, Dramsi S, Poyart C, Trieu-Cuot P, Kunst F, Glaser P. 2008. Shaping a bacterial genome by large chromosomal replacements, the evolutionary history of Streptococcus agalactiae. Proc Natl Acad Sci USA. 105(41):15961–15966.
  • Burrus V. 2017. Mechanisms of stabilization of integrative and conjugative elements. Curr Opin Microbiol. 38:44–50.
  • Burrus V, Marrero J, Waldor MK. 2006. The current ICE age: biology and evolution of SXT-related integrating conjugative elements. Plasmid. 55(3):173–183.
  • Burrus V, Pavlovic G, Decaris B, Guédon G. 2002. Conjugative transposons: the tip of the iceberg. Mol Microbiol. 46(3):601–610.
  • Burrus V, Quezada-Calvillo R, Marrero J, Waldor MK. 2006. SXT-related integrating conjugative element in new world Vibrio cholerae. Appl Environ Microbiol. 72(4):3054–3057.
  • Burrus V, Waldor MK. 2004. Formation of SXT Tandem Arrays and SXT-R391 Hybrids. J Bacteriol. 186(9):2636–2645.
  • Burrus V, Waldor MK. 2003. Control of SXT integration and excision. J Bacteriol. 185(17):5045–5054.
  • Burrus V, Waldor MK. 2004. Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol. 155(5):376–386.
  • Carraro N, Burrus V. 2014. Biology of three ICE families: SXT/R391, ICEBs1, and ICESt1/ICESt3. Microbiol Spectr. 2(6):1–20.
  • Carraro N, Burrus V. 2015. The dualistic nature of integrative and conjugative elements. Mob Genet Elements. 5(6):98–102.
  • Carraro N, Durand R, Rivard N, Anquetil C, Barrette C, Humbert M, Burrus V. 2017. Salmonella genomic island 1 (SGI1) reshapes the mating apparatus of IncC conjugative plasmids to promote self-propagation. PLoS Genet. 13(3):e1006705.
  • Carraro N, Libante V, Morel C, Charron-Bourgoin F, Leblond P, Guédon G. 2016. Plasmid-like replication of a minimal streptococcal integrative and conjugative element. Microbiology. 162(4):622–632.
  • Carraro N, Libante V, Morel C, Decaris B, Charron-Bourgoin F, Leblond P, Guédon G. 2011. Differential regulation of two closely related integrative and conjugative elements from Streptococcus thermophilus. BMC Microbiol. 11:238.
  • Carraro N, Matteau D, Luo P, Rodrigue S, Burrus V. 2014. The master activator of IncA/C conjugative plasmids stimulates genomic islands and multidrug resistance dissemination. PLoS Genet. 10(10):e1004714.
  • Carraro N, Poulin D, Burrus V. 2015. 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 Genet. 11(6):e1005298.
  • Carraro N, Richard X, Sulser S, Delavat F, Mazza C, van der Meer JR. 2020. An analog to digital converter controls bistable transfer competence development of a widespread bacterial integrative and conjugative element. Elife. 9: e57915
  • Carraro N, Rivard N, Ceccarelli D, Colwell RR, Burrus V. 2016. IncA/C conjugative plasmids mobilize a new family of multidrug resistance islands in clinical Vibrio cholerae non-O1/non-O139 isolates from Haiti. MBio. 7(4):e00509-16.
  • Ceccarelli D, Daccord A, René M, Burrus V. 2008. 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. 190(15):5328–5338.
  • Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. 2009. Structure of the outer membrane complex of a type IV secretion system. Nature. 462(7276):1011–1015.
  • Coetzee JN, Datta N, Hedges RW. 1972. R factors from Proteus rettgeri. J Gen Microbiol. 72(3):543–552.
  • Colombi E, Perry BJ, Sullivan JT, Bekuma AA, Terpolilli JJ, Ronson CW, Ramsay JP. 2021. Comparative analysis of integrative and conjugative mobile genetic elements in the genus Mesorhizobium. Microb Genomics. 7(10):e000657.
  • Croucher NJ, Mostowy R, Wymant C, Turner P, Bentley SD, Fraser C. 2016. Horizontal DNA transfer mechanisms of Bacteria as weapons of intragenomic conflict. PLoS Biol. 14(3):e1002394.
  • Cury J, Oliveira PH, De La Cruz F, Rocha EPC. 2018. Host range and genetic plasticity explain the coexistence of integrative and extrachromosomal mobile genetic elements. Mol Biol Evol. 35(9):2230–2239.
  • Daccord A, Ceccarelli D, Burrus V. 2010. Integrating conjugative elements of the SXT/R391 family trigger the excision and drive the mobilization of a new class of Vibrio genomic islands. Mol Microbiol. 78(3):576–588.
  • Daccord A, Ceccarelli D, Rodrigue S, Burrus V. 2013. Comparative analysis of mobilizable Genomic Islands. J Bacteriol. 195(3):606–614.
  • Daccord A, Mursell M, Poulin-Laprade D, Burrus V. 2012. Dynamics of the setCD-regulated integration and excision of genomic islands mobilized by integrating conjugative elements of the SXT/R391 family. J Bacteriol. 194(21):5794–5802.
  • Dalia AB, Seed KD, Calderwood SB, Camilli A. 2015. A globally distributed mobile genetic element inhibits natural transformation of Vibrio cholerae. Proc Natl Acad Sci USA. 112(33):10485–10490.
  • Delavat F, Miyazaki R, Carraro N, Pradervand N, van der Meer JR. 2017. The hidden life of integrative and conjugative elements. FEMS Microbiol Rev. 41(4):512–537.
  • Delavat F, Moritz R, van der Meer JR. 2019. Transient replication in specialized cells favors transfer of an integrative and conjugative element. MBio. 10(3):e01133-19.
  • Di Noto GP, Jara E, Iriarte A, Centrón D, Quiroga C. 2016. Genome analysis of a clinical isolate of Shewanella sp. uncovered an active hybrid integrative and conjugative element carrying an integron platform inserted in a novel genomic locus. Microbiology. 162(8):1335–1345.
  • Dik DA, Marous DR, Fisher JF, Mobashery S. 2017. Lytic transglycosylases: concinnity in concision of the bacterial cell wall. Crit Rev Biochem Mol Biol. 52(5):503–542.
  • Drenkard E, Ausubel FM. 2002. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature. 416(6882):740–743.
  • Dziewit L, Jazurek M, Drewniak L, Baj J, Bartosik D. 2007. 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. 189(5):1983–1997. 10.1128/JB.01610-06. 17158670
  • Frey KG, Bishop-Lilly KA, Daligault HE, Davenport KW, Bruce DC, Chain PS, Coyne SR, Chertkov O, Freitas T, Jaissle J, et al. 2014. Full-genome assembly of reference strain Providencia stuartii ATCC 33672. Genome Announc. 2(5):e01082-14.
  • Gaillard M, Vallaeys T, Vorhölter FJ, Minoia M, Werlen C, Sentchilo V, Pühler A, Van Meer JD. 2006. The clc element of Pseudomonas sp. strain B13, a genomic island with various catabolic properties. J Bacteriol. 188(5):1999–2013.
  • Garcillán-Barcia MP, de la Cruz F. 2008. Why is entry exclusion an essential feature of conjugative plasmids? Plasmid. 60(1):1–18.
  • Garcillán-Barcia MP, Alvarado A, De la Cruz F. 2011. Identification of bacterial plasmids based on mobility and plasmid population biology. FEMS Microbiol Rev. 35(5):936–956.
  • Garriss G, Poulin-Laprade D, Burrus V. 2013. DNA-damaging agents induce the RecA-independent homologous recombination functions of integrating conjugative elements of the SXT/R391 family. J Bacteriol. 195(9):1991–2003.
  • Garriss G, Waldor MK, Burrus V. 2009. Mobile antibiotic resistance encoding elements promote their own diversity. PLoS Genet. 5(12):e1000775.
  • Gerdes K, Moller-Jensen J, Jensen RB. 2000. Plasmid and chromosome partitioning: surprises from phylogeny. Mol Microbiol. 37(3):455–466.
  • Ghosh SK, Panda DK, Das J. 1989. Lack of umuDC gene functions in Vibrio cholerae cells. Mutation Research/fundamental and Molecular Mechanisms of Mutagenesis. 210(1):149–156. 10.1016/0027-5107(89)90054-7.
  • Giorgetti L, Siggers T, Tiana G, Caprara G, Notarbartolo S, Corona T, Pasparakis M, Milani P, Bulyk ML, Natoli G. 2010. Noncooperative interactions between transcription factors and clustered DNA binding sites enable graded transcriptional responses to environmental inputs. Mol Cell. 37(3):418–428.
  • Goldfarb T, Sberro H, Weinstock E, Cohen O, Doron S, Charpak‐Amikam Y, Afik S, Ofir G, Sorek R. 2015. BREX is a novel phage resistance system widespread in microbial genomes. Embo J. 34(2):169–183.
  • Guédon G, Libante V, Coluzzi C, Payot S, Leblond-Bourget N. 2017. The obscure world of integrative and mobilizable elements, highly widespread elements that pirate bacterial conjugative systems. Genes. 8(11):337.
  • Guglielmini J, Quintais L, Garcillán-Barcia MP, De La Cruz F, Rocha EPC. 2011. The repertoire of ICE in Prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet. 7(8):e1002222 10.1371/journal.pgen.1002222.
  • Guilloteau H, Pradalier C, Roman VL, Bellanger X, Billard P, Merlin C. 2021. Identification of antibiotics triggering the dissemination of antibiotic resistance genes by SXT/R391 elements using a dedicated high-throughput whole-cell biosensor assay. J Antimicrob Chemother. 77(1):112–123.
  • Hancock SJ, Phan MD, Luo Z, Lo AW, Peters KM, Nhu NTK, Forde BM, Whitfield J, Yang J, Strugnell RA, et al. 2020. Comprehensive analysis of IncC plasmid conjugation identifies a crucial role for the transcriptional regulator AcaB. Nat Microbiol. 5(11):1340–1348.
  • Harada S, Ishii Y, Saga T, Tateda K, Yamaguchi K. 2010. Chromosomally encoded blaCMY-2 located on a novel SXT/R391-related integrating conjugative element in a Proteus mirabilis clinical isolate. Antimicrob Agents Chemother. 54(9):3545–3550.
  • He D, Wang L, Zhao S, Liu L, Liu J, Hu G, Pan Y. 2020. A novel tigecycline resistance gene, tet(X6), on an SXT/R391 integrative and conjugative element in a Proteus genomospecies 6 isolate of retail meat origin. J Antimicrob Chemother. 75(5):1159–1164.
  • He J, Sun L, Zhang L, Leptihn S, Yu Y, Hua X. 2021. A novel SXT/R391 Integrative and Conjugative Element carries two copies of the blaNDM-1 gene in Proteus mirabilis. mSphere. 6(4):e00588–21.
  • Heather Z, Holden MTG, Steward KF, Parkhill J, Song L, Challis GL, Robinson C, Davis-Poynter N, Waller AS. 2008. A novel streptococcal integrative conjugative element involved in iron acquisition. Mol Microbiol. 70(5):1274–1292.
  • Hedges RW, Datta N, Coetzee JN, Dennison S. 1973. R factors from Proteus morganii. J Gen Microbiol. 77(2):249–259.
  • Hedges RW. 1975. R factors from Proteus mirabilis and P. vulgaris. J Gen Microbiol. 87(2):301–311.
  • Hedges RW. 1974. R factors from Providence. J Gen Microbiol. 81(1):171–181.
  • Ho C, Kulaeva OI, Levine AS, Woodgate R. 1993. A rapid method for cloning mutagenic DNA repair genes: isolation of umu- complementing genes from multidrug resistance plasmids R391, R446b, and R471a. J Bacteriol. 175(17):5411–5419.
  • Hochhut B, Beaber JW, Woodgate R, Waldor MK. 2001. Formation of chromosomal tandem arrays of the SXT element and R391, two conjugative chromosomally integrating elements that share an attachment site. J Bacteriol. 183(4):1124–1132.
  • Hochhut B, Marrero J, Waldor MK. 2000. Mobilization of plasmids and chromosomal DNA mediated by the SXT element, a constin found in Vibrio cholerae O139. J Bacteriol. 182(7):2043–2047.
  • Hochhut B, Waldor MK. 1999. Site-specific integration of the conjugal Vibrio cholerae SXT element into prfC. Mol Microbiol. 32(1):99–110.
  • Humbert M, Huguet KT, Coulombe F, Burrus V. 2019. Entry exclusion of conjugative plasmids of the IncA, IncC, and related untyped incompatibility groups. J Bacteriol. 201(10):e00731-18.
  • Jaskólska M, Adams DW, Blokesch M. 2022. Two defence systems eliminate plasmids from seventh pandemic Vibrio cholerae. Nature. 604(7905):323–329.
  • Jaszczur M, Bertram JG, Robinson A, Van Oijen AM, Woodgate R, Cox MM, Goodman MF. 2016. Mutations for worse or better: low-fidelity DNA synthesis by SOS DNA polymerase V is a tightly regulated double-edged sword. Biochemistry. 55(16):2309–2318.
  • Ji G, Silver S. 1992. Reduction of arsenate to arsenite by the ArsC protein of the arsenic resistance operon of Staphylococcus aureus plasmid pI258. Proc Natl Acad Sci USA. 89(20):9474–9478.
  • Johnson CM, Grossman AD. 2015. Integrative and Conjugative Elements (ICEs): What they do and how they work. Annu Rev Genet. 49:577–601.
  • Juíz-Río S, Osorio CR, de Lorenzo V, Lemos ML. 2005. Subtractive hybridization reveals a high genetic diversity in the fish pathogen Photobacterium damselae subsp. piscicida: evidence of a SXT-like element. Microbiology. 151(Pt 8):2659–2669.
  • Kong LH, Xiang R, Wang YL, Wu SK, Lei CW, Kang ZZ, Chen YP, Ye XL, Lai Y, Wang HN. 2020. Integration of the blaNDM-1 carbapenemase gene into a novel SXT/R391 integrative and conjugative element in Proteus vulgaris. J Antimicrob Chemother. 75(6):1439–1442.
  • Kulaeva OI, Wootton JC, Levine AS, Woodgate R. 1995. Characterization of the umu-complementing operon from R391. J Bacteriol. 177(10):2737–2743.
  • Kunito T, Kusano T, Oyaizu H, Senoo K, Kanazawa S, Matsumoto S. 1996. Cloning and sequence analysis of czc genes in Alcaligenes sp. Strain CT14. Biosci Biotechnol Biochem. 60(4):699–704.
  • Kutsukake K, Ohya Y, Iino T. 1990. Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol. 172(2):741–747.
  • Lee CA, Babic A, Grossman AD. 2010. Autonomous plasmid-like replication of a conjugative transposon. Mol Microbiol. 75(2):268–279.
  • LeGault KN, Hays SG, Angermeyer A, McKitterick AC, Johura F, Sultana M, Ahmed T, Alam M, Seed KD. 2021. Temporal shifts in antibiotic resistance elements govern phage-pathogen conflicts. Science. 373(6554):eabg2166.
  • Lei CW, Zhang AY, Wang HN, Liu BH, Yang LQ, Yang YQ. 2016. Characterization of SXT/R391 integrative and conjugative elements in Proteus mirabilis isolates from food-producing animals in China. Antimicrob Agents Chemother. 60(3):1935–1938.
  • Lewis JA, Hatfull GF. 2001. Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucleic Acids Res. 29(11):2205–2216.
  • Liu M, Li X, Xie Y, Bi D, Sun J, Li J, Tai C, Deng Z, Ou HY. 2019. ICEberg 2.0: an updated database of bacterial integrative and conjugative elements. Nucleic Acids Res. 47(D1):D660–D665.
  • Loenen WAM, Dryden DTF, Raleigh EA, Wilson GG, Murray NE. 2014. Highlights of the DNA cutters: a short history of the restriction enzymes. Nucleic Acids Res. 42(1):3–19.
  • Marrero J, Waldor MK. 2005. Interactions between inner membrane proteins in donor and recipient cells limit conjugal DNA transfer. Dev Cell. 8(6):963–970.
  • Marrero J, Waldor MK. 2007a. The SXT/R391 family of integrative conjugative elements is composed of two exclusion groups. J Bacteriol. 189(8):3302–3305.
  • Marrero J, Waldor MK. 2007b. Determinants of entry exclusion within Eex and TraG are cytoplasmic. J Bacteriol. 189(17):6469–6473.
  • Matthew M, Hedges RW, Smith JT. 1979. Types of β-lactamase determined by plasmids in gram-negative bacteria. J Bacteriol. 138(3):657–662.
  • McDonald JP, Quiros DR, Vaisman A, Mendez AR, Reyelt J, Schmidt M, Gonzalez M, Woodgate R. 2021. CroSR391, an ortholog of the λ Cro repressor, plays a major role in suppressing polVR391-dependent mutagenesis. Mol Microbiol. 116(3):877–889.
  • McGrath BM, O’Halloran JA, Pembroke JT. 2005. 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. 243(2):461–465.
  • McGrath BM, O’Halloran JA, Piterina AV, Pembroke JT. 2006. Molecular tools to detect the IncJ elements: a family of integrating, antibiotic resistant mobile genetic elements. J Microbiol Methods. 66(1):32–42.
  • McGrath BM, Pembroke JT. 2004. Detailed analysis of the insertion site of the mobile elements R997, pMERPH, R392, R705 and R391 in E. coli K12. FEMS Microbiol Lett. 237(1):19–26.
  • McGrew DA, Knight KL. 2003. Molecular design and functional organization of the RecA protein. Crit Rev Biochem Mol Biol. 38(5):385–432.
  • Mead S, Vaisman A, Valjavec-Gratian M, Karata K, Vandewiele D, Woodgate R. 2007. Characterization of polVR391: a Y-family polymerase encoded by rumAB from the IncJ conjugative transposon, R391. Mol Microbiol. 63(3):797–810.
  • Michael GB, Kadlec K, Sweeney MT, Brzuszkiewicz E, Liesegang H, Daniel R, Murray RW, Watts JL, Schwarz S. 2012. ICEPmu1, an integrative conjugative element (ICE) of Pasteurella multocida: analysis of the regions that comprise 12 antimicrobial resistance genes. J Antimicrob Chemother. 67(1):84–90.
  • Mohanraj RS, Mandal J. 2022. Azithromycin can induce SOS response and horizontal gene transfer of SXT element in Vibrio cholerae. Mol Biol Rep. 49(6):4737–4748.
  • Mucito-Varela E, Castillo-Rojas G, Calva JJ, López-Vidal Y. 2020. Integrative and Conjugative Elements of Helicobacter pylori are hypothetical virulence factors associated with gastric cancer. Front Cell Infect Microbiol. 10:525335.
  • Murphy DB, Pembroke JT. 1995. Transfer of the IncJ plasmid R391 to recombination deficient Escherichia coli K12: evidence that R391 behaves as a conjugal transposon. FEMS Microbiol Lett. 134(2-3):153–158.
  • Murphy DB, Pembroke JT. 1999. Monitoring of chromosomal insertions of the IncJ elements R391 and R997 in Escherichia coli K-12. FEMS Microbiol Lett. 174(2):355–361.
  • O’Halloran JA, McGrath BM, Pembroke JT. 2007. The orf4 gene of the enterobacterial ICE, R391, encodes a novel UV-inducible recombination directionality factor, Jef, involved in excision and transfer of the ICE. FEMS Microbiol Lett. 272(1):99–105.
  • Ohmori H, Friedberg EC, Fuchs RP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T, et al. 2001. The Y-family of DNA Polymerases. Mol Cell. 8(1):7–8.
  • Oliveira PH, Touchon M, Rocha EP. 2014. The interplay of restriction-modification systems with mobile genetic elements and their prokaryotic hosts. Nucleic Acids Research. 42(16):10618–10631. 10.1093/nar/gku734.
  • Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S. 2005. Switches in bacteriophage lambda development. Annu Rev Genet. 39:409–429.
  • Osorio CR, Marrero J, Wozniak RAF, Lemos ML, Burrus V, Waldor MK. 2008. Genomic and functional analysis of ICEPdaSpa1, a fish-pathogen-derived SXT-related integrating conjugative element that can mobilize a virulence plasmid. J Bacteriol. 190(9):3353–3361.
  • Pearson MM, Sebaihia M, Churcher C, Quail MA, Seshasayee AS, Luscombe NM, Abdellah Z, Arrosmith C, Atkin B, Chillingworth T, et al. 2008. Complete genome sequence of uropathogenic Proteus mirabilis, a master of both adherence and motility. J Bacteriol. 190(11):4027–4037.
  • Pembroke JT, MacMahon C, McGrath B. 2002. The role of conjugative transposons in Enterobacteriaceae. Cell Mol Life Sci. 59(12):2055–2064.
  • Pembroke JT, Murphy DB. 2000. Isolation and analysis of a circular form of the IncJ conjugative transposon-like elements, R391 and R997: implications for IncJ incompatibility. FEMS Microbiol Lett. 187(2):133–138.
  • Pembroke JT, Piterina AV. 2006. A novel ICE in the genome of Shewanella putrefaciens W3-18-1: comparison with the SXT/R391 ICE-like elements. FEMS Microbiol Lett. 264(1):80–88.
  • Pembroke JT, Stevens E, Brandsma JA, Van de Putte P. 1986. Location and cloning of the ultraviolet-sensitizing function from the chromosomally associated IncJ group plasmid, R391. Plasmid. 16(1):30–36.
  • Pembroke JT, Stevens E. 1984. The effect of plasmid R391 and other IncJ plasmids on the survival of Escherichia coli after UV irradiation. J Gen Microbiol. 130(7):1839–1844.
  • Peters SE, Hobman JL, Strike P, Ritchie DA. 1991. Novel mercury resistance determinants carried by IncJ plasmids pMERPH and R391. Mol Gen Genet. 228(1–2):294–299.
  • Poulin-Laprade D, Burrus V. 2015. A γ Cro-like repressor is essential for the induction of conjugative transfer of SXT/R391 elements in response to DNA damage. J Bacteriol. 197(24):3822–3833.
  • Poulin-Laprade D, Carraro N, Burrus V. 2015a. The extended regulatory networks of SXT/R391 integrative and conjugative elements and IncA/C conjugative plasmids. Front Microbiol. 6:837.
  • Poulin-Laprade D, Matteau D, Jacques PE, Rodrigue S, Burrus V. 2015b. Transfer activation of SXT/R391 integrative and conjugative elements: unraveling the SetCD regulon. Nucleic Acids Res. 43(4):2045–2056.
  • Ramsay JP, Bastholm TR, Verdonk CJ, Tambalo DD, Sullivan JT, Harold LK, Panganiban BA, Colombi E, Perry BJ, Jowsey W, et al. 2022. An epigenetic switch activates bacterial quorum sensing and horizontal transfer of an integrative and conjugative element. Nucleic Acids Res. 50(2):975–988.
  • Ramsay JP, Major AS, Komarovsky VM, Sullivan JT, Dy RL, Hynes MF, Salmond GPC, Ronson CW. 2013. A widely conserved molecular switch controls quorum sensing and symbiosis island transfer in Mesorhizobium loti through expression of a novel antiactivator. Mol Microbiol. 87(1):1–13.
  • Ramsay JP, Sullivan JT, Stuart GS, Lamont IL, Ronson CW. 2006. Excision and transfer of the Mesorhizobium loti R7A symbiosis island requires an integrase IntS, a novel recombination directionality factor RdfS, and a putative relaxase RlxS. Mol Microbiol. 62(3):723–734.
  • Rice LB. 1998. Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob Agents Chemother. 42(8):1871–1877.
  • Rice LB, Carias LL, Rudin S, Hutton RA, Marshall S. 2010. Multiple copies of functional, Tet(M)-encoding Tn916-like elements in a clinical Enterococcus faecium isolate. Plasmid. 64(3):150–155.
  • Rivard N, Colwell RR, Burrus V. 2020. Antibiotic resistance in Vibrio cholerae: mechanistic Insights from IncC plasmid-mediated dissemination of a Novel Family of Genomic Islands Inserted at trmE. mSphere. 5(4):e00748-20.
  • Roberts AP, Mullany P. 2011. Tn916-like genetic elements: a diverse group of modular mobile elements conferring antibiotic resistance. FEMS Microbiol Rev. 35(5):856–871.
  • Rocha EPC. 2016. Using sex to cure the genome. PLoS Biol. 14(3):e1002417.
  • Rodríguez-Blanco A, Lemos ML, Osorio CR. 2012. Integrating conjugative elements as vectors of antibiotic, mercury, and quaternary ammonium compound resistance in marine aquaculture environments. Antimicrob Agents Chemother. 56(5):2619–2626.
  • Roman VL, Merlin C, Baron S, Larvor E, Le Devendec L, Virta MPJ, Bellanger X. 2021. Abundance and environmental host range of the SXT/R391 ICEs in aquatic environmental communities. Environ Pollut. 288:117673.
  • Roy D, Huguet KT, Grenier F, Burrus V. 2020. IncC conjugative plasmids and SXT/R391 elements repair double-strand breaks caused by CRISPR-Cas during conjugation. Nucleic Acids Res. 48(16):8815–8827.
  • Ryan MP, Armshaw P, O’Halloran JA, Pembroke JT. 2017. Analysis and comparative genomics of R997, the first SXT/R391 integrative and conjugative element (ICE) of the Indian Sub-Continent. Sci Rep. 7(1):8562.
  • Ryan MP, Armshaw P, Pembroke JT. 2016. SXT/R391 integrative and conjugative elements (ICEs) encode a novel “trap-door” strategy for mobile element escape. Front Microbiol. 7:829.
  • Ryan MP, Pembroke JT, Adley CC. 2009. Novel Tn4371-ICE like element in Ralstonia pickettii and Genome mining for comparative elements. BMC Microbiol. 9:242.
  • Ryan MP, Slattery S, Pembroke JT. 2019. A novel arsenate‐resistant determinant associated with ICEpMERPH, a member of the SXT/R391 group of mobile genetic elements. Genes. 10(12):1048.
  • Sato JL, Fonseca MRB, Cerdeira LT, Tognim MCB, Sincero TCM, Noronha Do Amaral MC, Lincopan N, Galhardo RS. 2020. Genomic analysis of SXT/R391 Integrative Conjugative Elements from Proteus mirabilis isolated in Brazil. Front Microbiol. 1110.3389/fmicb.2020.571472.
  • Sato JL, Fonseca DLdH, Galhardo RS. 2022. rumAB genes from SXT/R391 ICEs confer UV-induced mutability to Proteus mirabilis hosts and improve conjugation after UV irradiation. DNA Repair. 112:103297 10.1016/j.dnarep.2022.103297.
  • Sedgwick SG, Ho C, Woodgate R. 1991. Mutagenic DNA repair in enterobacteria. J Bacteriol. 173(18):5604–5611. 10.1128/jb.173.18.5604-5611.1991.
  • Sentchilo V, Czechowska K, Pradervand N, Minoia M, Miyazaki R, Van Der Meer JR. 2009. Intracellular excision and reintegration dynamics of the ICEclc genomic island of Pseudomonas knackmussii sp. strain B13. Mol Microbiol. 72(5):1293–1306.
  • Seth-Smith HMB, Fookes MC, Okoro CK, Baker S, Harris SR, Scott P, Pickard D, Quail MA, Churcher C, Sanders M, et al. 2012. Structure, diversity, and mobility of the salmonella pathogenicity island 7 family of integrative and conjugative elements within enterobacteriaceae. J Bacteriol. 194(6):1494–1504.
  • Seth-Smith H, Croucher NJ. 2009. Genome watch: breaking the ICE. Nat Rev Microbiol. 7(5):328–329.
  • Slattery S, Tony Pembroke J, Murnane JG, Ryan MP. 2020. Isolation, nucleotide sequencing and genomic comparison of a Novel SXT/R391 ICE mobile genetic element isolated from a municipal wastewater environment. Sci Rep. 10(1):8716.
  • Smyth DS, Robinson DA. 2009. Integrative and sequence characteristics of a novel genetic element, ICE6013, in Staphylococcus aureus. J Bacteriol. 191(19):5964–5975.
  • Song Z, Zuo L, Li C, Tian Y, Wang H. 2020. Copper ions facilitate the conjugative transfer of SXT/R391 integrative and conjugative element across bacterial genera. Front Microbiol. 11:616792.
  • Spagnoletti M, Ceccarelli D, Rieux A, Fondi M, Taviani E, Fani R, Colombo MM, Colwell RR, Balloux F. 2014. Acquisition and evolution of SXT-R391 integrative conjugative elements in the seventh-pandemic Vibrio cholerae lineage. MBio. 5(4):e01356-14.
  • Sullivan JT, Ronson CW. 1998. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci USA. 95(9):5145–5149.
  • Sullivan JT, Trzebiatowski JR, Cruickshank RW, Gouzy J, Brown SD, Elliot RM, Fleetwood DJ, McCallum NG, Rossbach U, Stuart GS, et al. 2002. Comparative sequence analysis of the symbiosis island of Mesorhizobium loti strain R7A. J Bacteriol. 184(11):3086–3095.
  • Szekeres ES, Woodgate R, Lawrence CW. 1996. Substitution of mucAB or rumAB for umuDC alters the relative frequencies of the two classes of mutations induced by a site-specific T-T cyclobutane dimer and the efficiency of translesion DNA synthesis. J Bacteriol. 178(9):2559–2563.
  • Taviani E, Grim CJ, Chun J, Huq A, Colwell RR. 2009. Genomic analysis of a novel integrative conjugative element in Vibrio cholerae. FEBS Lett. 583(22):3630–3636.
  • Te Poele EM, Bolhuis H, Dijkhuizen L. 2008. Actinomycete integrative and conjugative elements, Antonie Van Leeuwenhoek. Int J Gen Mol Microbiol. 94(1):127–143.
  • Tischler AD, Camilli A. 2004. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol. 53(3):857–869.
  • Toussaint A, Merlin C, Monchy S, Benotmane MA, Leplae R, Mergeay M, Springael D. 2003. The biphenyl- and 4-chlorobiphenyl-catabolic transposon Tn4371, a member of a new family of genomic islands related to IncP and Ti plasmids. Appl Environ Microbiol. 69(8):4837–4845.
  • Tuffin IM, de Groot P, Deane SM, Rawlings DE. 2005. An unusual Tn21-like transposon containing an ars operon is present in highly arsenic-resistant strains of the biomining bacterium Acidithiobacillus caldus. Microbiology (Reading). 151(Pt 9):3027–3039.
  • Van Houdt P, Toussaint A, Ryan MP, Pembroke JT, Mergeay M, Adley CC. 2011. The Tn4371 ICE family of bacterial mobile genetic elements. In: Roberts A, Mullany P, editors. Bacterial integrative mobile genetic elements. Austin: Landes Bioscience; p. 179–200.
  • Van Melderen L. 2010. Toxin-antitoxin systems: Why so many, what for? Curr Opin Microbiol. 13(6):781–785.
  • Waldor MK, Tschäpe H, Mekalanos JJ. 1996. A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139. J Bacteriol. 178(14):4157–4165.
  • Wozniak RAF, Fouts DE, Spagnoletti M, Colombo MM, Ceccarelli D, Garriss G, Déry C, Burrus V, Waldor MK. 2009. Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet. 5(12):e1000786.
  • Wozniak RAF, Waldor MK. 2010. Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol. 8(8):552–563.
  • Wozniak RAF, Waldor MK. 2009. A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet. 5(3):e1000439.
  • Wright LD, Grossman AD. 2016. Autonomous replication of the conjugative transposon Tn916. J Bacteriol. 198(24):3355–3366.
  • Xiong A, Jayaswal RK. 1998. Molecular characterization of a chromosomal determinant conferring resistance to zinc and cobalt ions in Staphylococcus aureus. J Bacteriol. 180(16):4024–4029.
  • Yamamoto T, Nair GB, Albert MJ, Parodi CC, Takeda Y. 1995. Survey of in vitro susceptibilities of Vibrio cholerae O1 and O139 to antimicrobial agents. Antimicrob Agents Chemother. 39(1):241–244.
  • Yokota T, Kuwahara S. 1977. Temperature sensitive R plasmid obtained from naturally isolated drug resistant Vibrio cholerae (biotype El Tor). Antimicrob Agents Chemother. 11(1):13–20.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.