The High Pathogenicity Island of Yersinia pseudotuberculosis IP32637 was previously shown to be horizontally transferable as part of a large chromosomal segment. We demonstrate here that at low temperature other chromosomal loci, as well as a non-mobilizable plasmid (pUC4K), are also transferable. This transfer, designated GDT4 (Generalized DNA Transfer at 4°C), required the presence of an IP32637 endogenous plasmid (pGDT4) that carries several mobile genetic elements and a conjugation machinery. We established that cure of this plasmid or inactivation of its sex pilus fully abrogates this process. Analysis of the mobilized pUC4K recovered from transconjugants revealed the insertion of one of the pGDT4–borne ISs, designated ISYps1, at different sites on the transferred plasmid molecules. This IS belongs to the IS6 family, which moves by replicative transposition, and thus could drive the formation of cointegrates between pGDT4 and the host chromosome and could mediate the transfer of chromosomal regions in an Hfr-like manner. In support of this model, we show that a suicide plasmid carrying ISYps1 is able to integrate itself, flanked by ISYps1 copies, at multiple locations into the Escherichia coli chromosome. Furthermore, we demonstrate the formation of RecA-independent cointegrates between the ISYps1-harboring plasmid and an ISYps1-free replicon, leading to the passive transfer of the non-conjugative plasmid. We thus demonstrate here a natural mechanism of horizontal gene exchange, which is less constrained and more powerful than the classical Hfr mechanism, as it only requires the presence of an IS6-type element on a conjugative replicon to drive the horizontal transfer of any large block of plasmid or chromosomal DNA. This natural mechanism of chromosome transfer, which occurs under conditions mimicking those found in the environment, may thus play a significant role in bacterial evolution, pathogenesis, and adaptation to new ecological niches.
Vyšlo v časopise: A Natural System of Chromosome Transfer in. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002529 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002529
1. CarnielEGuilvoutIPrenticeM 1996 Characterization of a large chromosomal “high-pathogenicity island” in biotype 1B Yersinia enterocolitica. J Bacteriol 178 6743 6751
2. HeesemannJHantkeKVockeTSakenERakinA 1993 Virulence of Yersinia enterocolitica Is Closely Associated with Siderophore Production, Expression of an Iron-Repressible Outer Membrane Polypeptide of 65000 Da and Pesticin Sensitivity. Mol Microbiol 8 397 408
3. LesicBCarnielE 2005 Horizontal transfer of the high-pathogenicity island of Yersinia pseudotuberculosis. J Bacteriol 187 3352 3358
4. LesicBCarnielE 2004 The High-Pathogenicity Island: a broad-host-range pathogenicity island. CarnielEHinnebuschJ Yersinia: Molecular and Cellular Biology: Horizon Bioscience 285 306
5. LesicBBachSGhigoJMDobrindtUHackerJ 2004 Excision of the high-pathogenicity island of Yersinia pseudotuberculosis requires the combined actions of its cognate integrase and Hef, a new recombination directionality factor. Mol Microbiol 52 1337 1348
6. SchubertSDarluPClermontOWieserAMagistroG 2009 Role of intraspecies recombination in the spread of pathogenicity islands within the Escherichia coli species. PLoS Pathog 5 e1000257 doi:10.1371/journal.ppat.1000257
7. MansonJMHancockLEGilmoreMS 2010 Mechanism of chromosomal transfer of Enterococcus faecalis pathogenicity island, capsule, antimicrobial resistance, and other traits. Proc Natl Acad Sci USA 107 12269 12274
8. ChainPSCarnielELarimerFWLamerdinJStoutlandPO 2004 Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci USA 101 13826 13831
9. SimonetMMazighDBercheP 1984 Growth of Yersinia pseudotuberculosis in mouse spleen despite loss of a virulence plasmid of mol. wt 47×106. J Med Microbiol 18 371 375
10. AchtmanMZurthKMorelliCTorreaGGuiyouleA 1999 Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci USA 96 14043 14048
11. HurstMRBecherSAO'CallaghanM 2011 Nucleotide sequence of the Serratia entomophila plasmid pADAP and the Serratia proteamaculans pU143 plasmid virulence associated region. Plasmid 65 32 41
12. SmillieCGarcillan-BarciaMPFranciaMVRochaEPde la CruzF 2010 Mobility of plasmids. Microbiol Mol Biol Rev 74 434 452
13. FranciaMVVarsakiAGarcillan-BarciaMPLatorreADrainasC 2004 A classification scheme for mobilization regions of bacterial plasmids. FEMS Microbiol Rev 28 79 100
14. Garcillan-BarciaMPFranciaMVde la CruzF 2009 The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33 657 687
15. SnellingsNJPopekMLindlerLE 2001 Complete DNA sequence of Yersinia enterocolitica serotype 0∶8 low-calcium-response plasmid reveals a new virulence plasmid-associated replicon. Infect Immun 69 4627 4638
16. ChainPSCarnielELarimerFWLamerdinJStoutlandPO 2004 Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci USA 101 13826 13831
17. MahillonJChandlerM 1998 Insertion sequences. Microbiol Mol Biol Rev 62 725 774
18. SundstromLRadstromPSwedbergGSkoldO 1988 Site-specific recombination promotes linkage between trimethoprim - and sulfonamide resistance genes. Sequence characterization of dhfrV and sulI and a recombination active locus of Tn21. Mol Gen Genet 213 191 201
19. MaherDTaylorDE 1993 Host range and transfer efficiency of incompatibility group HI plasmids. Can J Microbiol 39 581 587
20. FornsNBanosRCBalsalobreCJuarezAMadridC 2005 Temperature-dependent conjugative transfer of R27: role of chromosome - and plasmid-encoded Hha and H-NS proteins. J Bacteriol 187 3950 3959
21. CornelisGRSluitersCDelorIGeibDKanigaK 1991 ymoA, a Yersinia enterocolitica chromosomal gene modulating the expression of virulence functions. Mol Microbiol 5 1023 1034
22. OnoSGoldbergMDOlssonTEspositoDHintonJC 2005 H-NS is a part of a thermally controlled mechanism for bacterial gene regulation. Biochem J 391 203 213
23. TendengCBertinPN 2003 H-NS in Gram-negative bacteria: a family of multifaceted proteins. Trends Microbiol 11 511 518
24. ZhouDSQinLHanYPQiuJFChenZL 2006 Global analysis of iron assimilation and fur regulation in Yersinia pestis. FEMS Microbiol Lett 258 9 17
25. HanYPZhouDSPangXZhangLSongYJ 2005 DNA microarray analysis of the heat - and cold-shock stimulons in Yersinia pestis. Microbes Infect 7 335 348
26. SamuelsALLankaEDaviesJE 2000 Conjugative junctions in RP4-mediated mating of Escherichia coli. J Bacteriol 182 2709 2715
27. DurrenbergerMBVilligerWBachiT 1991 Conjugational junctions: morphology of specific contacts in conjugating Escherichia coli bacteria. J Struct Biol 107 146 156
28. BrandlMT 2006 Fitness of human enteric pathogens on plants and implications for food safety. Annu Rev Phytopathol 44 367 392
29. JoshuaGWKarlyshevAVSmithMPIsherwoodKETitballRW 2003 A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology 149 3221 3229
30. BradleyDE 1980 Morphological and serological relationships of conjugative pili. Plasmid 4 155 169
31. BradleyDETaylorDECohenDR 1980 Specification of surface mating systems among conjugative drug resistance plasmids in Escherichia coli K-12. J Bacteriol 143 1466 1470
32. ZhongXKrolJETopEMKroneSM 2010 Accounting for mating pair formation in plasmid population dynamics. J Theor Biol 262 711 719
33. TopEMergeayMSpringaelDVerstraeteW 1990 Gene escape model: transfer of heavy metal resistance genes from Escherichia coli to Alcaligenes eutrophus on agar plates and in soil samples. Appl Environ Microbiol 56 2471 2479
34. UmedaMOhtsuboE 1989 Mapping of insertion elements IS1, IS2 and IS3 on the Escherichia coli K-12 chromosome. Role of the insertion elements in formation of Hfrs and F' factors and in rearrangement of bacterial chromosomes. J Mol Biol 208 601 614
35. CrisonaNJNowakJANagaishiHClarkAJ 1980 Transposon-mediated conjugational transmission of nonconjugative plasmids. J Bacteriol 142 701 713
36. StrauchEHoffmannBHeinsGAppelB 2000 Isolation of a new insertion element of Yersinia intermedia closely related to remnants of mobile genetic elements present on Yersinia plasmids harboring the Yop virulon. FEMS Microbiol Lett 193 37 44
37. OhtsuboEZenilmanMOhtsuboH 1980 Plasmids containing insertion elements are potential transposons. Proc Natl Acad Sci USA 77 750 754
38. WollmanELJacobFHayesW 1956 Conjugation and genetic recombination in Escherichia coli K-12. Cold Spring Harb Symp Quant Biol 21 141 162
39. HayesW 1953 The mechanism of genetic recombination in Escherichia coli. Cold Spring Harb Symp Quant Biol 18 75 93
40. LederbergJTatumEL 1946 Gene recombination in Escherichia coli. Nature 158 558
41. JacobFWollmanE 1961 Sexuality and the Genetics of Bacteria New York Academic Press
42. CurtissR3rdStallionsDR 1969 Probability of F integration and frequency of stable Hfr donors in F+ populations of Escherichia coli K-12. Genetics 63 27 38
43. MatneyTSGoldschmidtEPErwinNSScroggsRA 1964 A preliminary map of genomic sites for F-attachment in Escherichia coli K12. Biochem Biophys Res Commun 17 278 281
44. CurtissRMacrinaFFalkinhamI 1974 Escherichia coli-An overview; KingRC New York Plenum Press 115 135
45. WillettsNSCrowtherCHollowayBW 1981 The insertion sequence IS21 of R68.45 and the molecular basis for mobilization of the bacterial chromosome. Plasmid 6 30 52
46. HaasDHollowayBW 1978 Chromosome mobilization by the R plasmid R68.45: a tool in Pseudomonas genetics. Mol Gen Genet 158 229 237
47. Van GijsegemFToussaintA 1982 Chromosome transfer and R-prime formation by an RP4::mini-Mu derivative in Escherichia coli, Salmonella typhimurium, Klebsiella pneumoniae, and Proteus mirabilis. Plasmid 7 30 44
48. Ramirez-ArcosSFernandez-HerreroLAMarinIBerenguerJ 1998 Anaerobic growth, a property horizontally transferred by an Hfr-like mechanism among extreme thermophiles. J Bacteriol 180 3137 3143
49. GassonMJGodonJJPillidgeCJEatonTJJuryK 1995 Characterization of conjugation in Lactococcus lactis. Int Dairy J 5 757 762
50. PettisGSCohenSN 1994 Transfer of the plJ101 plasmid in Streptomyces lividans requires a cis-acting function dispensable for chromosomal gene transfer. Mol Microbiol 13 955 964
51. BuchrieserCGlaserPRusniokCNedjariHD'HautevilleH 2000 The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri. Mol Microbiol 38 760 771
52. DemarreGGueroutA-MMatsumoto-MashimoCRowe-MagnusDAMarlièreDAMazelD 2005 A new family of mobilizable suicide plasmids based on broad host range R388 plasmid (IncW) and RP4 plasmid (IncPalpha) conjugative machineries and their cognate Escherichia coli host strains. Res Microbiol 156 245 255
53. DerbiseALesicBDacheuxDGhigoJMCarnielE 2003 A rapid and simple method for inactivating chromosomal genes in Yersinia. FEMS Immunol Med Microbiol Immunol 38 113 116
54. FleischmannRDAdamsMDWhiteOClaytonRAKirknessEF 1995 Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269 496 512
55. GordonDAbajianCGreenP 1998 Consed: a graphical tool for sequence finishing. Genome Res 8 195 202
56. EwingBGreenP 1998 Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res 8 186 194
57. BabicAGueroutAMMazelD 2008 Construction of an improved RP4 (RK2)-based conjugative system. Res Microbiol 159 545 549
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
