Plasmid Flux in ST131 Sublineages, Analyzed by Plasmid Constellation Network (PLACNET), a New Method for Plasmid Reconstruction from Whole Genome Sequences

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Plasmids are difficult to analyze in WGS datasets, due to the fragmented nature of the obtained sequences. We developed a method, called PLACNET, which greatly facilitates this analysis. As an example, we analyzed the plasmidome of E. coli ST131, an ExPEC clonal group involved in human urinary tract infections and septicemia. Relevant variation within this clone (e.g., antibiotic resistance and virulence) is frequently caused by the acquisition and loss of plasmids and other mobile genetic elements. Nevertheless, our knowledge of the ST131 plasmidome is limited to a few antibiotic resistance plasmids and to identification of replicons from known plasmid groups. PLACNET analysis extends the number of sequenced plasmids in ST131, which can be used for comparative genomics, from 11 to 50. The ST131 plasmidome is seemingly huge, encompassing roughly 50% of the main plasmid groups of γ–proteobacteria. MOBF12/IncF plasmids are apparently the most active players in the dissemination of relevant genetic information.

Vyšlo v časopise: Plasmid Flux in ST131 Sublineages, Analyzed by Plasmid Constellation Network (PLACNET), a New Method for Plasmid Reconstruction from Whole Genome Sequences. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004766
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004766

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Zdroje

1. DidelotX, BowdenR, WilsonDJ, PetoTE, CrookDW (2012) Transforming clinical microbiology with bacterial genome sequencing. Nat Rev Genet 13: 601–612.

2. JohnsonTJ, NolanLK (2009) Pathogenomics of the virulence plasmids of Escherichia coli. Microbiol Mol Biol Rev 73: 750–774.

3. CarattoliA (2011) Plasmids in Gram negatives: molecular typing of resistance plasmids. Int J Med Microbiol 301: 654–658.

4. CarattoliA (2013) Plasmids and the spread of resistance. Int J Med Microbiol 303: 298–304.

5. AhmedSA, AwosikaJ, BaldwinC, Bishop-LillyKA, BiswasB, et al. (2012) Genomic comparison of Escherichia coli O104:H4 isolates from 2009 and 2011 reveals plasmid, and prophage heterogeneity, including shiga toxin encoding phage stx2. PLoS One 7: e48228.

6. BoerlinP, ChenS, ColbourneJK, JohnsonR, De GrandisS, et al. (1998) Evolution of enterohemorrhagic Escherichia coli hemolysin plasmids and the locus for enterocyte effacement in shiga toxin-producing E. coli. Infect Immun 66: 2553–2561.

7. CouturierM, BexF, BergquistPL, MaasWK (1988) Identification and classification of bacterial plasmids. Microbiol Rev 52: 375–395.

8. CarattoliA, BertiniA, VillaL, FalboV, HopkinsKL, et al. (2005) Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 63: 219–228.

9. VillaL, Garcia-FernandezA, FortiniD, CarattoliA (2010) Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother 65: 2518–2529.

10. Garcia-FernandezA, FortiniD, VeldmanK, MeviusD, CarattoliA (2009) Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother 63: 274–281.

11. AlvaradoA, Garcillan-BarciaMP, de la CruzF (2012) A Degenerate Primer MOB Typing (DPMT) Method to Classify Gamma-Proteobacterial Plasmids in Clinical and Environmental Settings. PLoS One 7: e40438.

12. EdwardsDJ, HoltKE (2013) Beginner's guide to comparative bacterial genome analysis using next-generation sequence data. Microb Inform Exp 3: 2.

13. PriceLB, JohnsonJR, AzizM, ClabotsC, JohnstonB, et al. (2013) The epidemic of extended-spectrum-beta-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. MBio 4: e00377–00313.

14. JohnsonJR, ClermontO, JohnstonB, ClabotsC, TchesnokovaV, et al. (2014) Rapid and specific detection, molecular epidemiology, and experimental virulence of the O16 subgroup within Escherichia coli sequence type 131. J Clin Microbiol.

15. BlancV, Leflon-GuiboutV, BlancoJ, HaenniM, MadecJY, et al. (2014) Prevalence of day-care centre children (France) with faecal CTX-M-producing Escherichia coli comprising O25b:H4 and O16:H5 ST131 strains. J Antimicrob Chemother.

16. PettyNK, Ben ZakourNL, Stanton-CookM, SkippingtonE, TotsikaM, et al. (2014) Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci U S A.

17. CoqueTM, NovaisA, CarattoliA, PoirelL, PitoutJ, et al. (2008) Dissemination of clonally related Escherichia coli strains expressing extended-spectrum beta-lactamase CTX-M-15. Emerg Infect Dis 14: 195–200.

18. Nicolas-ChanoineMH, BertrandX, MadecJY (2014) Escherichia coli ST131, an Intriguing Clonal Group. Clin Microbiol Rev 27: 543–574.

19. Nicolas-ChanoineMH, BlancoJ, Leflon-GuiboutV, DemartyR, AlonsoMP, et al. (2008) Intercontinental emergence of Escherichia coli clone O25:H4-ST131 producing CTX-M-15. J Antimicrob Chemother 61: 273–281.

20. Leflon-GuiboutV, BlancoJ, AmaqdoufK, MoraA, GuizeL, et al. (2008) Absence of CTX-M enzymes but high prevalence of clones, including clone ST131, among fecal Escherichia coli isolates from healthy subjects living in the area of Paris, France. J Clin Microbiol 46: 3900–3905.

21. PlatellJL, JohnsonJR, CobboldRN, TrottDJ (2011) Multidrug-resistant extraintestinal pathogenic Escherichia coli of sequence type ST131 in animals and foods. Vet Microbiol 153: 99–108.

22. AlbrechtovaK, DolejskaM, CizekA, TausovaD, KlimesJ, et al. (2012) Dogs of nomadic pastoralists in northern Kenya are reservoirs of plasmid-mediated cephalosporin- and quinolone-resistant Escherichia coli, including pandemic clone B2-O25-ST131. Antimicrob Agents Chemother 56: 4013–4017.

23. HernandezJ, BonnedahlJ, EliassonI, WallenstenA, ComstedtP, et al. (2010) Globally disseminated human pathogenic Escherichia coli of O25b-ST131 clone, harbouring blaCTX-M-15, found in Glaucous-winged gull at remote Commander Islands, Russia. Environ Microbiol Rep 2: 329–332.

24. PallecchiL, BartoloniA, FiorelliC, MantellaA, Di MaggioT, et al. (2007) Rapid dissemination and diversity of CTX-M extended-spectrum beta-lactamase genes in commensal Escherichia coli isolates from healthy children from low-resource settings in Latin America. Antimicrob Agents Chemother 51: 2720–2725.

25. MoraA, HerreraA, MamaniR, LopezC, AlonsoMP, et al. (2010) Recent emergence of clonal group O25b:K1:H4-B2-ST131 ibeA strains among Escherichia coli poultry isolates, including CTX-M-9-producing strains, and comparison with clinical human isolates. Appl Environ Microbiol 76: 6991–6997.

26. DhanjiH, MurphyNM, AkhigbeC, DoumithM, HopeR, et al. (2011) Isolation of fluoroquinolone-resistant O25b:H4-ST131 Escherichia coli with CTX-M-14 extended-spectrum beta-lactamase from UK river water. J Antimicrob Chemother 66: 512–516.

27. Colomer-LluchM, MoraA, LopezC, MamaniR, DahbiG, et al. (2013) Detection of quinolone-resistant Escherichia coli isolates belonging to clonal groups O25b:H4-B2-ST131 and O25b:H4-D-ST69 in raw sewage and river water in Barcelona, Spain. J Antimicrob Chemother 68: 758–765.

28. GibreelTM, DodgsonAR, CheesbroughJ, BoltonFJ, FoxAJ, et al. (2012) High metabolic potential may contribute to the success of ST131 uropathogenic Escherichia coli. J Clin Microbiol 50: 3202–3207.

29. NovaisA, PiresJ, FerreiraH, CostaL, MontenegroC, et al. (2012) Characterization of globally spread Escherichia coli ST131 isolates (1991 to 2010). Antimicrob Agents Chemother 56: 3973–3976.

30. BlancoJ, MoraA, MamaniR, LopezC, BlancoM, et al. (2011) National survey of Escherichia coli causing extraintestinal infections reveals the spread of drug-resistant clonal groups O25b:H4-B2-ST131, O15:H1-D-ST393 and CGA-D-ST69 with high virulence gene content in Spain. J Antimicrob Chemother 66: 2011–2021.

31. JohnsonJR, KuskowskiMA, GajewskiA, SahmDF, KarlowskyJA (2004) Virulence characteristics and phylogenetic background of multidrug-resistant and antimicrobial-susceptible clinical isolates of Escherichia coli from across the United States, 2000-2001. J Infect Dis 190: 1739–1744.

32. SchubertS, DarluP, ClermontO, WieserA, MagistroG, et al. (2009) Role of intraspecies recombination in the spread of pathogenicity islands within the Escherichia coli species. PLoS Pathog 5: e1000257.

33. WirthT, FalushD, LanR, CollesF, MensaP, et al. (2006) Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60: 1136–1151.

34. JohnsonJR, Nicolas-ChanoineMH, DebRoyC, CastanheiraM, RobicsekA, et al. (2012) Comparison of Escherichia coli ST131 pulsotypes, by epidemiologic traits, 1967–2009. Emerg Infect Dis 18: 598–607.

35. JohnsonJR, TchesnokovaV, JohnstonB, ClabotsC, RobertsPL, et al. (2013) Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli. J Infect Dis 207: 919–928.

36. BlancoJ, MoraA, MamaniR, LopezC, BlancoM, et al. (2013) Four main virotypes among extended-spectrum-beta-lactamase-producing isolates of Escherichia coli O25b:H4-B2-ST131: bacterial, epidemiological, and clinical characteristics. J Clin Microbiol 51: 3358–3367.

37. PeiranoG, PitoutJD (2014) Fluoroquinolone resistant Escherichia coli ST131 causing bloodstream infections in a centralized Canadian region: the rapid emergence of H30-Rx sublineage. Antimicrob Agents Chemother.

38. ColpanA, JohnstonB, PorterS, ClabotsC, AnwayR, et al. (2013) Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans. Clin Infect Dis 57: 1256–1265.

39. BanerjeeR, RobicsekA, KuskowskiMA, PorterS, JohnstonBD, et al. (2013) Molecular epidemiology of Escherichia coli sequence type 131 and Its H30 and H30-Rx subclones among extended-spectrum-beta-lactamase-positive and -negative E. coli clinical isolates from the Chicago Region, 2007 to 2010. Antimicrob Agents Chemother 57: 6385–6388.

40. DahbiG, MoraA, LopezC, AlonsoMP, MamaniR, et al. (2013) Emergence of new variants of ST131 clonal group among extraintestinal pathogenic Escherichia coli producing extended-spectrum beta-lactamases. Int J Antimicrob Agents 42: 347–351.

41. AvasthiTS, KumarN, BaddamR, HussainA, NandanwarN, et al. (2011) Genome of multidrug-resistant uropathogenic Escherichia coli strain NA114 from India. J Bacteriol 193: 4272–4273.

42. TotsikaM, BeatsonSA, SarkarS, PhanMD, PettyNK, et al. (2011) Insights into a Multidrug Resistant Escherichia coli Pathogen of the Globally Disseminated ST131 Lineage: Genome Analysis and Virulence Mechanisms. PLoS One 6: e26578.

43. ClarkG, PaszkiewiczK, HaleJ, WestonV, ConstantinidouC, et al. (2012) Genomic analysis uncovers a phenotypically diverse but genetically homogeneous Escherichia coli ST131 clone circulating in unrelated urinary tract infections. J Antimicrob Chemother 67: 868–877.

44. LavigneJP, VergunstAC, GoretL, SottoA, CombescureC, et al. (2012) Virulence potential and genomic mapping of the worldwide clone Escherichia coli ST131. PLoS One 7: e34294.

45. KunneC, BillionA, MshanaSE, SchmiedelJ, DomannE, et al. (2012) Complete sequences of plasmids from the hemolytic-uremic syndrome-associated Escherichia coli strain HUSEC41. J Bacteriol 194: 532–533.

46. GradYH, GodfreyP, CerquieraGC, Mariani-KurkdjianP, GoualiM, et al. (2013) Comparative genomics of recent Shiga toxin-producing Escherichia coli O104:H4: short-term evolution of an emerging pathogen. MBio 4: e00452–00412.

47. BrunderW, SchmidtH, FroschM, KarchH (1999) The large plasmids of Shiga-toxin-producing Escherichia coli (STEC) are highly variable genetic elements. Microbiology 145 (Pt 5): 1005–1014.

48. PallenMJ, WrenBW (2007) Bacterial pathogenomics. Nature 449: 835–842.

49. KeenEC (2012) Paradigms of pathogenesis: targeting the mobile genetic elements of disease. Front Cell Infect Microbiol 2: 161.

50. WoodfordN, TurtonJF, LivermoreDM (2011) Multiresistant Gram-negative bacteria: the role of high-risk clones in the dissemination of antibiotic resistance. FEMS Microbiol Rev 35: 736–755.

51. BlancoM, AlonsoMP, Nicolas-ChanoineMH, DahbiG, MoraA, et al. (2009) Molecular epidemiology of Escherichia coli producing extended-spectrum {beta}-lactamases in Lugo (Spain): dissemination of clone O25b:H4-ST131 producing CTX-M-15. J Antimicrob Chemother 63: 1135–1141.

52. CoelhoA, MoraA, MamaniR, LopezC, Gonzalez-LopezJJ, et al. (2011) Spread of Escherichia coli O25b:H4-B2-ST131 producing CTX-M-15 and SHV-12 with high virulence gene content in Barcelona (Spain). J Antimicrob Chemother 66: 517–526.

53. Garcillan-BarciaMP, AlvaradoA, de la CruzF (2011) Identification of bacterial plasmids based on mobility and plasmid population biology. FEMS Microbiol Rev 35: 936–956.

54. HauserM, MayerCE, SodingJ (2013) kClust: fast and sensitive clustering of large protein sequence databases. BMC Bioinformatics 14: 248.

55. PeigneC, BidetP, Mahjoub-MessaiF, PlainvertC, BarbeV, et al. (2009) The plasmid of Escherichia coli strain S88 (O45:K1:H7) that causes neonatal meningitis is closely related to avian pathogenic E. coli plasmids and is associated with high-level bacteremia in a neonatal rat meningitis model. Infect Immun 77: 2272–2284.

56. ZongZ (2013) Complete sequence of pJIE186-2, a plasmid carrying multiple virulence factors from a sequence type 131 Escherichia coli O25 strain. Antimicrob Agents Chemother 57: 597–600.

57. FalgenhauerL, YaoY, FritzenwankerM, SchmiedelJ, ImirzaliogluC, et al. (2014) Complete Genome Sequence of Phage-Like Plasmid pECOH89, Encoding CTX-M-15. Genome Announc 2.

58. MiquelS, PeyretailladeE, ClaretL, de ValleeA, DossatC, et al. (2010) Complete genome sequence of Crohn's disease-associated adherent-invasive E. coli strain LF82. PLoS One 5.

59. KidgellC, PickardD, WainJ, JamesK, Diem NgaLT, et al. (2002) Characterisation and distribution of a cryptic Salmonella typhi plasmid pHCM2. Plasmid 47: 159–171.

60. KimM, KimS, RyuS (2012) Complete genome sequence of bacteriophage SSU5 specific for Salmonella enterica serovar Typhimurium rough strains. J Virol 86: 10894.

61. CottellJL, WebberMA, ColdhamNG, TaylorDL, Cerdeno-TarragaAM, et al. (2011) Complete sequence and molecular epidemiology of IncK epidemic plasmid encoding blaCTX-M-14. Emerg Infect Dis 17: 645–652.

62. ValverdeA, CantonR, Garcillan-BarciaMP, NovaisA, GalanJC, et al. (2009) Spread of bla(CTX-M-14) is driven mainly by IncK plasmids disseminated among Escherichia coli phylogroups A, B1, and D in Spain. Antimicrob Agents Chemother 53: 5204–5212.

63. KimSR, KomanoT (1992) Nucleotide sequence of the R721 shufflon. J Bacteriol 174: 7053–7058.

64. MellataM, MadduxJT, NamT, ThomsonN, HauserH, et al. (2012) New insights into the bacterial fitness-associated mechanisms revealed by the characterization of large plasmids of an avian pathogenic E. coli. PLoS One 7: e29481.

65. WangP, XiongY, LanR, YeC, WangH, et al. (2011) pO157_Sal, a novel conjugative plasmid detected in outbreak isolates of Escherichia coli O157:H7. J Clin Microbiol 49: 1594–1597.

66. TouchonM, HoedeC, TenaillonO, BarbeV, BaeriswylS, et al. (2009) Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet 5: e1000344.

67. BrownCJ, SenD, YanoH, BauerML, RogersLM, et al. (2013) Diverse broad-host-range plasmids from freshwater carry few accessory genes. Appl Environ Microbiol 79: 7684–7695.

68. SmajsD, MicenkovaL, SmardaJ, VrbaM, SevcikovaA, et al. (2010) Bacteriocin synthesis in uropathogenic and commensal Escherichia coli: colicin E1 is a potential virulence factor. BMC Microbiol 10: 288.

69. BaqueroF, CoqueTM (2011) Multilevel population genetics in antibiotic resistance. FEMS Microbiol Rev 35: 705–706.

70. RaskoDA, RosovitzMJ, MyersGS, MongodinEF, FrickeWF, et al. (2008) The pangenome structure of Escherichia coli: comparative genomic analysis of E. coli commensal and pathogenic isolates. J Bacteriol 190: 6881–6893.

71. HazenTH, SahlJW, FraserCM, DonnenbergMS, ScheutzF, et al. (2013) Refining the pathovar paradigm via phylogenomics of the attaching and effacing Escherichia coli. Proc Natl Acad Sci U S A 110: 12810–12815.

72. SkippingtonE, RaganMA (2011) Lateral genetic transfer and the construction of genetic exchange communities. FEMS Microbiol Rev.

73. OguraY, OokaT, IguchiA, TohH, AsadulghaniM, et al. (2009) Comparative genomics reveal the mechanism of the parallel evolution of O157 and non-O157 enterohemorrhagic Escherichia coli. Proc Natl Acad Sci U S A 106: 17939–17944.

74. CroucherNJ, HarrisSR, GradYH, HanageWP (2013) Bacterial genomes in epidemiology—present and future. Philos Trans R Soc Lond B Biol Sci 368: 20120202.

75. JohnsonTJ, LogueCM, JohnsonJR, KuskowskiMA, SherwoodJS, et al. (2012) Associations Between Multidrug Resistance, Plasmid Content, and Virulence Potential Among Extraintestinal Pathogenic and Commensal Escherichia coli from Humans and Poultry. Foodborne Pathog Dis 9: 37–46.

76. PolzMF, AlmEJ, HanageWP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet 29: 170–175.

77. ReevesPR, LiuB, ZhouZ, LiD, GuoD, et al. (2011) Rates of mutation and host transmission for an Escherichia coli clone over 3 years. PLoS One 6: e26907.

78. SandegrenL, LinkeviciusM, LytsyB, MelhusA, AnderssonDI (2012) Transfer of an Escherichia coli ST131 multiresistance cassette has created a Klebsiella pneumoniae-specific plasmid associated with a major nosocomial outbreak. J Antimicrob Chemother 67: 74–83.

79. ChenL, HuH, ChavdaKD, ZhaoS, LiuR, et al. (2014) Complete Sequence of a KPC-Producing IncN Multidrug-Resistant Plasmid from an Epidemic Escherichia coli Sequence Type 131 Strain in China. Antimicrob Agents Chemother 58: 2422–2425.

80. PartridgeSR, ZongZ, IredellJR (2011) Recombination in IS26 and Tn2 in the evolution of multiresistance regions carrying blaCTX-M-15 on conjugative IncF plasmids from Escherichia coli. Antimicrob Agents Chemother 55: 4971–4978.

81. O'HaraJA, HuF, AhnC, NelsonJ, RiveraJI, et al. (2014) Molecular Epidemiology of KPC-Producing Escherichia coli: Occurrence of ST131-fimH30 Subclone Harboring pKpQIL-like IncFIIk Plasmid. Antimicrob Agents Chemother.

82. JohnsonTJ, WannemuehlerYM, JohnsonSJ, LogueCM, WhiteDG, et al. (2007) Plasmid replicon typing of commensal and pathogenic Escherichia coli isolates. Appl Environ Microbiol 73: 1976–1983.

83. ChenL, ChavdaKD, Al LahamN, MelanoRG, JacobsMR, et al. (2013) Complete nucleotide sequence of a blaKPC-harboring IncI2 plasmid and its dissemination in New Jersey and New York hospitals. Antimicrob Agents Chemother 57: 5019–5025.

84. JohnsonTJ, LangKS (2012) IncA/C plasmids: An emerging threat to human and animal health? Mob Genet Elements 2: 55–58.

85. KimYA, QureshiZA, Adams-HaduchJM, ParkYS, ShuttKA, et al. (2012) Features of infections due to Klebsiella pneumoniae carbapenemase-producing Escherichia coli: emergence of sequence type 131. Clin Infect Dis 55: 224–231.

86. MuniesaM, Colomer-LluchM, JofreJ (2013) Potential impact of environmental bacteriophages in spreading antibiotic resistance genes. Future Microbiol 8: 739–751.

87. Hoyland-KroghsboNM, MaerkedahlRB, SvenningsenSL (2013) A quorum-sensing-induced bacteriophage defense mechanism. MBio 4: e00362–00312.

88. SchimkeRT (1984) Gene amplification in cultured animal cells. Cell 37: 705–713.

89. BaqueroF, TedimAP, CoqueTM (2013) Antibiotic resistance shaping multi-level population biology of bacteria. Front Microbiol 4: 15.

90. Andersen PS, Stegger M, Aziz M, Contente-Cuomo T, Gibbons HS, et al. (2013) Complete Genome Sequence of the Epidemic and Highly Virulent CTX-M-15-Producing H30-Rx Subclone of Escherichia coli ST131. Genome Announc 1.

91. TohH, OshimaK, ToyodaA, OguraY, OokaT, et al. (2010) Complete genome sequence of the wild-type commensal Escherichia coli strain SE15, belonging to phylogenetic group B2. J Bacteriol 192: 1165–1166.

92. BoydDA, TylerS, ChristiansonS, McGeerA, MullerMP, et al. (2004) Complete nucleotide sequence of a 92-kilobase plasmid harboring the CTX-M-15 extended-spectrum beta-lactamase involved in an outbreak in long-term-care facilities in Toronto, Canada. Antimicrob Agents Chemother 48: 3758–3764.

93. WoodfordN, CarattoliA, KarisikE, UnderwoodA, EllingtonMJ, et al. (2009) Complete nucleotide sequences of plasmids pEK204, pEK499, and pEK516, encoding CTX-M enzymes in three major Escherichia coli lineages from the United Kingdom, all belonging to the international O25:H4-ST131 clone. Antimicrob Agents Chemother 53: 4472–4482.

94. PartridgeSR, EllemJA, TetuSG, ZongZ, PaulsenIT, et al. (2011) Complete sequence of pJIE143, a pir-type plasmid carrying ISEcp1-blaCTX-M-15 from an Escherichia coli ST131 isolate. Antimicrob Agents Chemother 55: 5933–5935.

95. LiW, GodzikA (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22: 1658–1659.

96. DarlingAE, MauB, PernaNT (2010) progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 5: e11147.

97. Capella-GutierrezS, Silla-MartinezJM, GabaldonT (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25: 1972–1973.

98. StamatakisA (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690.

99. ZerbinoDR, BirneyE (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829.

100. LangmeadB, SalzbergSL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.

101. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.

102. CamachoC, CoulourisG, AvagyanV, MaN, PapadopoulosJ, et al. (2009) BLAST+: architecture and applications. BMC Bioinformatics 10: 421.

103. Garcillan-BarciaMP, de la CruzF (2013) Ordering the bestiary of genetic elements transmissible by conjugation. Mob Genet Elements 3: e24263.

104. del SolarG, GiraldoR, Ruiz-EchevarriaMJ, EspinosaM, Diaz-OrejasR (1998) Replication and control of circular bacterial plasmids. Microbiol Mol Biol Rev 62: 434–464.

105. ZhengJ, PengD, RuanL, SunM (2013) Evolution and dynamics of megaplasmids with genome sizes larger than 100 kb in the Bacillus cereus group. BMC Evol Biol 13: 262.

106. OsbornAM, da Silva TatleyFM, SteynLM, PickupRW, SaundersJR (2000) Mosaic plasmids and mosaic replicons: evolutionary lessons from the analysis of genetic diversity in IncFII-related replicons. Microbiology 146 (Pt 9): 2267–2275.

107. SmillieC, Garcillan-BarciaMP, FranciaMV, RochaEP, de la CruzF (2010) Mobility of plasmids. Microbiol Mol Biol Rev 74: 434–452.

108. BesemerJ, LomsadzeA, BorodovskyM (2001) GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29: 2607–2618.

109. GuglielminiJ, QuintaisL, Garcillan-BarciaMP, de la CruzF, RochaEP (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation. PLoS Genet 7: e1002222.

110. EddySR (2011) Accelerated Profile HMM Searches. PLoS Comput Biol 7: e1002195.

111. SmootME, OnoK, RuscheinskiJ, WangPL, IdekerT (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431–432.

112. ZhouY, CallDR, BroschatSL (2013) Using protein clusters from whole proteomes to construct and augment a dendrogram. Adv Bioinformatics 2013: 191586.

113. TekaiaF, LazcanoA, DujonB (1999) The genomic tree as revealed from whole proteome comparisons. Genome Res 9: 550–557.

114. TekaiaF, YeramianE (2005) Genome trees from conservation profiles. PLoS Comput Biol 1: e75.

115. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. (2013) vegan: Community Ecology Package.

116. ParadisE, ClaudeJ, StrimmerK (2004) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics 20: 289–290.

117. AlikhanNF, PettyNK, Ben ZakourNL, BeatsonSA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12: 402.

118. AssefaS, KeaneTM, OttoTD, NewboldC, BerrimanM (2009) ABACAS: algorithm-based automatic contiguation of assembled sequences. Bioinformatics 25: 1968–1969.

119. BonninRA, PoirelL, CarattoliA, NordmannP (2012) Characterization of an IncFII plasmid encoding NDM-1 from Escherichia coli ST131. PLoS One 7: e34752.

120. CullikA, PfeiferY, PragerR, von BaumH, WitteW (2010) A novel IS26 structure surrounds blaCTX-M genes in different plasmids from German clinical Escherichia coli isolates. J Med Microbiol 59: 580–587.

121. ChenL, ChavdaKD, MelanoRG, JacobsMR, KollB, et al. (2014) Comparative Genomic Analysis of KPC-Encoding pKpQIL-Like Plasmids and Their Distribution in New Jersey and New York Hospitals. Antimicrob Agents Chemother 58: 2871–2877.