The Repertoire of ICE in Prokaryotes Underscores the Unity, Diversity, and Ubiquity of Conjugation
Horizontal gene transfer shapes the genomes of prokaryotes by allowing rapid acquisition of novel adaptive functions. Conjugation allows the broadest range and the highest gene transfer input per transfer event. While conjugative plasmids have been studied for decades, the number and diversity of integrative conjugative elements (ICE) in prokaryotes remained unknown. We defined a large set of protein profiles of the conjugation machinery to scan over 1,000 genomes of prokaryotes. We found 682 putative conjugative systems among all major phylogenetic clades and showed that ICEs are the most abundant conjugative elements in prokaryotes. Nearly half of the genomes contain a type IV secretion system (T4SS), with larger genomes encoding more conjugative systems. Surprisingly, almost half of the chromosomal T4SS lack co-localized relaxases and, consequently, might be devoted to protein transport instead of conjugation. This class of elements is preponderant among small genomes, is less commonly associated with integrases, and is rarer in plasmids. ICEs and conjugative plasmids in proteobacteria have different preferences for each type of T4SS, but all types exist in both chromosomes and plasmids. Mobilizable elements outnumber self-conjugative elements in both ICEs and plasmids, which suggests an extensive use of T4SS in trans. Our evolutionary analysis indicates that switch of plasmids to and from ICEs were frequent and that extant elements began to differentiate only relatively recently. According to the present results, ICEs are the most abundant conjugative elements in practically all prokaryotic clades and might be far more frequently domesticated into non-conjugative protein transport systems than previously thought. While conjugative plasmids and ICEs have different means of genomic stabilization, their mechanisms of mobility by conjugation show strikingly conserved patterns, arguing for a unitary view of conjugation in shaping the genomes of prokaryotes by horizontal gene transfer.
Vyšlo v časopise:
The Repertoire of ICE in Prokaryotes Underscores the Unity, Diversity, and Ubiquity of Conjugation. PLoS Genet 7(8): e32767. doi:10.1371/journal.pgen.1002222
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002222
Souhrn
Horizontal gene transfer shapes the genomes of prokaryotes by allowing rapid acquisition of novel adaptive functions. Conjugation allows the broadest range and the highest gene transfer input per transfer event. While conjugative plasmids have been studied for decades, the number and diversity of integrative conjugative elements (ICE) in prokaryotes remained unknown. We defined a large set of protein profiles of the conjugation machinery to scan over 1,000 genomes of prokaryotes. We found 682 putative conjugative systems among all major phylogenetic clades and showed that ICEs are the most abundant conjugative elements in prokaryotes. Nearly half of the genomes contain a type IV secretion system (T4SS), with larger genomes encoding more conjugative systems. Surprisingly, almost half of the chromosomal T4SS lack co-localized relaxases and, consequently, might be devoted to protein transport instead of conjugation. This class of elements is preponderant among small genomes, is less commonly associated with integrases, and is rarer in plasmids. ICEs and conjugative plasmids in proteobacteria have different preferences for each type of T4SS, but all types exist in both chromosomes and plasmids. Mobilizable elements outnumber self-conjugative elements in both ICEs and plasmids, which suggests an extensive use of T4SS in trans. Our evolutionary analysis indicates that switch of plasmids to and from ICEs were frequent and that extant elements began to differentiate only relatively recently. According to the present results, ICEs are the most abundant conjugative elements in practically all prokaryotic clades and might be far more frequently domesticated into non-conjugative protein transport systems than previously thought. While conjugative plasmids and ICEs have different means of genomic stabilization, their mechanisms of mobility by conjugation show strikingly conserved patterns, arguing for a unitary view of conjugation in shaping the genomes of prokaryotes by horizontal gene transfer.
Zdroje
1. OchmanHLawrenceJGGroismanEA 2000 Lateral gene transfer and the nature of bacterial innovation. Nature 405 299 304
2. de la CruzFDaviesJ 2000 Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol 8 128 133
3. TettelinHRileyDCattutoCMediniD 2008 Comparative genomics: the bacterial pan-genome. Curr Opin Microbiol 11 472 477
4. LorenzMGWackernagelW 1994 Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 58 563 602
5. BrochetMRusniokCCouveEDramsiSPoyartC 2008 Shaping a bacterial genome by large chromosomal replacements, the evolutionary history of Streptococcus agalactiae. Proc Natl Acad Sci U S A 105 15961 15966
6. NormanAHansenLHSorensenSJ 2009 Conjugative plasmids: vessels of the communal gene pool. Philos Trans R Soc Lond B Biol Sci 364 2275 2289
7. HalarySLeighJWCheaibBLopezPBaptesteE 2010 Network analyses structure genetic diversity in independent genetic worlds. Proc Natl Acad Sci U S A 107 127 132
8. KloesgesTPopaOMartinWDaganT 2011 Networks of Gene Sharing among 329 Proteobacterial Genomes Reveal Differences in Lateral Gene Transfer Frequency at Different Phylogenetic Depths. Mol Biol Evol 28 1057 1074
9. Amábile-CuevasCFChicurelME 1992 Bacterial plasmids and gene flux. Cell 70 189 199
10. SebaihiaMWrenBWMullanyPFairweatherNFMintonN 2006 The multidrug-resistant human pathogen Clostridium difficile has a highly mobile, mosaic genome. Nat Genet 38 779 786
11. ThomasCM 2000 Horizontal Gene Pool: Bacterial Plasmids and Gene Spread Amsterdam CRC 444
12. van der MeerJRSentchiloV 2003 Genomic islands and the evolution of catabolic pathways in bacteria. Curr Opin Biotechnol 14 248 254
13. de la CruzFFrostLSMeyerRJZechnerE 2010 Conjugative DNA Metabolism in Gram-negative Bacteria. FEMS Microbiol Rev 34 18 40
14. SmillieCGarcillan-BarciaMPFranciaMVRochaEPde la CruzF 2010 Mobility of plasmids. Microbiol Mol Biol Rev 74 434 452
15. ThompsonDVMelchersLSIdlerKBSchilperoortRAHooykaasPJ 1988 Analysis of the complete nucleotide sequence of the Agrobacterium tumefaciens virB operon. Nucleic Acids Res 16 4621 4636
16. LawleyTDKlimkeWAGubbinsMJFrostLS 2003 F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 224 1 15
17. SampeiGFuruyaNTachibanaKSaitouYSuzukiT 2010 Complete genome sequence of the incompatibility group I1 plasmid R64. Plasmid 64 92 103
18. JuhasMCrookDWDimopoulouIDLunterGHardingRM 2007 Novel type IV secretion system involved in propagation of genomic islands. J Bacteriol 189 761 771
19. BurrusVPavlovicGDecarisBGuedonG 2002 Conjugative transposons: the tip of the iceberg. Mol Microbiol 46 601 610
20. WozniakRAWaldorMK 2010 Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat Rev Microbiol 8 552 563
21. HochhutBWaldorMK 1999 Site-specific integration of the conjugal Vibrio cholerae SXT element into prfC. Mol Microbiol 32 99 110
22. RavatnRStuderSZehnderAJvan der MeerJR 1998 Int-B13, an unusual site-specific recombinase of the bacteriophage P4 integrase family, is responsible for chromosomal insertion of the 105-kilobase clc element of Pseudomonas sp. Strain B13. J Bacteriol 180 5505 5514
23. CaparonMGScottJR 1989 Excision and insertion of the conjugative transposon Tn916 involves a novel recombination mechanism. Cell 59 1027 1034
24. RajeevLMalanowskaKGardnerJF 2009 Challenging a paradigm: the role of DNA homology in tyrosine recombinase reactions. Microbiol Mol Biol Rev 73 300 309
25. BrochetMDa CunhaVCouveERusniokCTrieu-CuotP 2009 Atypical association of DDE transposition with conjugation specifies a new family of mobile elements. Mol Microbiol 71 948 959
26. WangHMullanyP 2000 The large resolvase TndX is required and sufficient for integration and excision of derivatives of the novel conjugative transposon Tn5397. J Bacteriol 182 6577 6583
27. ChumleyFGMenzelRRothJR 1979 Hfr formation directed by tn10. Genetics 91 639 655
28. CaseyJDalyCFitzgeraldGF 1991 Chromosomal integration of plasmid DNA by homologous recombination in Enterococcus faecalis and Lactococcus lactis subsp. lactis hosts harboring Tn919. Appl Environ Microbiol 57 2677 2682
29. LeeCABabicAGrossmanAD 2010 Autonomous plasmid-like replication of a conjugative transposon. Mol Microbiol 75 268 279
30. DoubletBBoydDMulveyMRCloeckaertA 2005 The Salmonella genomic island 1 is an integrative mobilizable element. Mol Microbiol 55 1911 1924
31. DouardGPraudKCloeckaertADoubletB 2010 The Salmonella genomic island 1 is specifically mobilized in trans by the IncA/C multidrug resistance plasmid family. PLoS ONE 5 e15302 doi:10.1371/journal.pone.0015302
32. DaccordACeccarelliDBurrusV 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 78 576 588
33. AntonenkaUNoltingCHeesemannJRakinA 2005 Horizontal transfer of Yersinia high-pathogenicity island by the conjugative RP4 attB target-presenting shuttle plasmid. Mol Microbiol 57 727 734
34. DobrindtUHochhutBHentschelUHackerJ 2004 Genomic islands in pathogenic and environmental microorganisms. Nat Rev Microbiol 2 414 424
35. HofreuterDOdenbreitSHaasR 2001 Natural transformation competence in Helicobacter pylori is mediated by the basic components of a type IV secretion system. Mol Microbiol 41 379 391
36. LlosaMRoyCDehioC 2009 Bacterial type IV secretion systems in human disease. Mol Microbiol 73 141 151
37. FrankACAlsmarkCMThollessonMAnderssonSG 2005 Functional divergence and horizontal transfer of type IV secretion systems. Mol Biol Evol 22 1325 1336
38. JuhasMPowerPMHardingRMFergusonDJDimopoulouID 2007 Sequence and functional analyses of Haemophilus spp. genomic islands. Genome Biol 8 R237
39. WozniakRAFoutsDESpagnolettiMColomboMMCeccarelliD 2009 Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet 5 e1000786 doi:10.1371/journal.pgen.1000786
40. EddySR 1998 Profile hidden Markov models. Bioinformatics 14 755 763
41. BurrusVWaldorMK 2004 Shaping bacterial genomes with integrative and conjugative elements. Res Microbiol 155 376 386
42. SmithCJParkerAC 1993 Identification of a circular intermediate in the transfer and transposition of Tn4555, a mobilizable transposon from Bacteroides spp. J Bacteriol 175 2682 2691
43. ShoemakerNBWangGRStevensAMSalyersAA 1993 Excision, transfer, and integration of NBU1, a mobilizable site-selective insertion element. J Bacteriol 175 6578 6587
44. GrohmannEMuthGEspinosaM 2003 Conjugative plasmid transfer in gram-positive bacteria. Microbiol Mol Biol Rev 67 277 301
45. VogelmannJAmmelburgMFingerCGuezguezJLinkeD 2011 Conjugal plasmid transfer in Streptomyces resembles bacterial chromosome segregation by FtsK/SpoIIIE. Embo J 30 2246 2254
46. VogelJAndrewsHWongSIsbergR 1998 Conjugative transfer by the virulence system of Legionella pneumophila. Science 279 873 876
47. SeubertAHiestandRde la CruzFDehioC 2003 A bacterial conjugation machinery recruited for pathogenesis. Mol Microbiol 49 1253 1266
48. de PazHDSangariFJBollandSGarcia-LoboJMDehioC 2005 Functional interactions between type IV secretion systems involved in DNA transfer and virulence. Microbiology 151 3505 3516
49. BlancGOgataHRobertCAudicSClaverieJM 2007 Lateral gene transfer between obligate intracellular bacteria: evidence from the Rickettsia massiliae genome. Genome Res 17 1657 1664
50. MarendaMBarbeVGourguesGMangenotSSagneE 2006 A new integrative conjugative element occurs in Mycoplasma agalactiae as chromosomal and free circular forms. J Bacteriol 188 4137 4141
51. WeinertLWelchJFMJ 2009 Conjugation genes are common throughout the genus Rickettsia and are transmitted horizontally. Proc Biol Sci 276 3619 3627
52. PrangishviliDAlbersSHolzIArnoldHStedmanK 1998 Conjugation in archaea: frequent occurrence of conjugative plasmids in Sulfolobus. Plasmid 40 190 202
53. StedmanKMSheQPhanHHolzISinghH 2000 pING family of conjugative plasmids from the extremely thermophilic archaeon Sulfolobus islandicus: insights into recombination and conjugation in Crenarchaeota. J Bacteriol 182 7014 7020
54. SalyersAAShoemakerNBStevensAMLiLY 1995 Conjugative transposons: an unusual and diverse set of integrated gene transfer elements. Microbiol Rev 59 579 590
55. MerlinCSpringaelDToussaintA 1999 Tn4371: A modular structure encoding a phage-like integrase, a Pseudomonas-like catabolic pathway, and RP4/Ti-like transfer functions. Plasmid 41 40 54
56. SullivanJTRonsonCW 1998 Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc Natl Acad Sci U S A 95 5145 5149
57. KlockgetherJRevaOLarbigKTummlerB 2004 Sequence analysis of the mobile genome island pKLC102 of Pseudomonas aeruginosa C. J Bacteriol 186 518 534
58. GaillardMVallaeysTVorholterFJMinoiaMWerlenC 2006 The clc element of Pseudomonas sp. strain B13, a genomic island with various catabolic properties. J Bacteriol 188 1999 2013
59. ChoNHKimHRLeeJHKimSYKimJ 2007 The Orientia tsutsugamushi genome reveals massive proliferation of conjugative type IV secretion system and host-cell interaction genes. Proc Natl Acad Sci U S A 104 7981 7986
60. ParkhillJSebaihiaMPrestonAMurphyLDThomsonN 2003 Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35 32 40
61. Alvarez-MartinezCEChristiePJ 2009 Biological diversity of prokaryotic type IV secretion systems. Microbiol Mol Biol Rev 73 775 808
62. EngelPSalzburgerWLieschMChangCCMaruyamaS 2011 Parallel Evolution of a Type IV Secretion System in Radiating Lineages of the Host-Restricted Bacterial Pathogen Bartonella. PLoS Genet 7 e1001296 doi:10.1371/journal.pgen.1001296
63. FischerWWindhagerLRohrerSZeillerMKarnholzA 2010 Strain-specific genes of Helicobacter pylori: genome evolution driven by a novel type IV secretion system and genomic island transfer. Nucleic Acids Res 38 6089 6101
64. NystedtBFrankACThollessonMAnderssonSG 2008 Diversifying selection and concerted evolution of a type IV secretion system in Bartonella. Mol Biol Evol 25 287 300
65. MediniDCovacciADonatiC 2006 Protein homology network families reveal step-wise diversification of Type III and Type IV secretion systems. PLoS Comput Biol 2 e173 doi:10.1371/journal.pcbi.0020173
66. NaumMBrownEWMason-GamerRJ 2009 Phylogenetic evidence for extensive horizontal gene transfer of type III secretion system genes among enterobacterial plant pathogens. Microbiology 155 3187 3199
67. Garcillan-BarciaMPFranciaMVde la CruzF 2009 The diversity of conjugative relaxases and its application in plasmid classification. FEMS Microbiol Rev 33 657 687
68. PrestonGM 2007 Metropolitan microbes: type III secretion in multihost symbionts. Cell Host Microbe 2 291 294
69. LacroixBTzfiraTVainsteinACitovskyV 2006 A case of promiscuity: Agrobacterium's endless hunt for new partners. Trends Genet 22 29 37
70. RoccoJMChurchwardG 2006 The integrase of the conjugative transposon Tn916 directs strand- and sequence-specific cleavage of the origin of conjugal transfer, oriT, by the endonuclease Orf20. J Bacteriol 188 2207 2213
71. XuJBjursellMKHimrodJDengSCarmichaelLK 2003 A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299 2074 2076
72. EdgarRC 2004 MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32 1792 1797
73. AnisimovaMGascuelO 2006 Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 55 539 552
74. GouyMGuindonSGascuelO 2010 SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27 221 224
75. StamatakisA 2006 RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22 2688 2690
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2011 Číslo 8
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- An EMT–Driven Alternative Splicing Program Occurs in Human Breast Cancer and Modulates Cellular Phenotype
- Chromosome Painting Reveals Asynaptic Full Alignment of Homologs and HIM-8–Dependent Remodeling of Chromosome Territories during Meiosis
- Discovery of Sexual Dimorphisms in Metabolic and Genetic Biomarkers
- Regulation of p53/CEP-1–Dependent Germ Cell Apoptosis by Ras/MAPK Signaling