Cited by 41Bacterial Genetics and BiotechnologyAntibiotic Resistance in BacteriaGenomics and Phylogenetic Studies

Genetic exchanges are more frequent in bacteria encoding capsules

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Rendueles, Olaya, de Sousa, Jorge A. Moura, Bernheim, Aude, Touchon, Marie, Rocha, Eduardo P. C.·2018·PLOS Genetics

Abstract

Capsules allow bacteria to colonize novel environments, to withstand numerous stresses, and to resist antibiotics. Yet, even though genetic exchanges with other cells should be adaptive under such circumstances, it has been suggested that capsules lower the rates of homologous recombination and horizontal gene transfer. We analysed over one hundred pan-genomes and thousands of bacterial genomes for the evidence of an association between genetic exchanges (or lack thereof) and the presence of a capsule system. We found that bacteria encoding capsules have larger pan-genomes, higher rates of horizontal gene transfer, and higher rates of homologous recombination in their core genomes. Accordingly, genomes encoding capsules have more plasmids, conjugative elements, transposases, prophages, and integrons. Furthermore, capsular loci are frequent in plasmids, and can be found in prophages. These results are valid for Bacteria, independently of their ability to be naturally transformable. Since we have shown previously that capsules are commonly present in nosocomial pathogens, we analysed their co-occurrence with antibiotic resistance genes. Genomes encoding capsules have more antibiotic resistance genes, especially those encoding efflux pumps, and they constitute the majority of the most worrisome nosocomial bacteria. We conclude that bacteria with capsule systems are more genetically diverse and have fast-evolving gene repertoires, which may further contribute to their success in colonizing novel niches such as humans under antibiotic therapy.

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  • Causal inference methods such as phylogenetic path analysis could be used to test causal hypotheses.

    “In this case, causal inference methods such as phylogenetic path analysis could be used to test causal hypotheses84,88,89.”

    From A phylogenetic approach to comparative genomics (2025) · cites this paper as [89]

    The Discussion proposes alternative causal explanations for the association between capsules and genetic exchange. However, neither it nor the Methods passages found when searching for phylogenetic path analysis and causal inference say that path analysis could be used to test causal hypotheses. No page numbers are available in our copy. (LLM, conf=0.76)

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  1. [1]Yother J. Capsules of Streptococcus pneumoniae and other bacteria: paradigms for polysaccharide biosynthesis and regulation. Annu Rev Microbiol. 2011; 65: 563– 81. 10.1146/annurev.micro.62.081307.162944. 21721938 · DOI
  2. [2]Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annual review of biochemistry. 2006; 75: 39– 68. 10.1146/annurev.biochem.75.103004.142545. 16756484 · DOI
  3. [3]Candela T, Fouet A. Poly-gamma-glutamate in bacteria. Mol Microbiol. 2006; 60(5): 1091– 8. 10.1111/j.1365-2958.2006.05179.x. 16689787 · DOI · Paper page
  4. [4]Lam TT, Claus H, Frosch M, Vogel U. Sequence analysis of serotype-specific synthesis regions II of Haemophilus influenzae serotypes c and d: evidence for common ancestry of capsule synthesis in Pasteurellaceae and Neisseria meningitidis. Res Microbiol. 2011; 162(5): 483– 7. 10.1016/j.resmic.2011.04.002. 21513796 · DOI
  5. [5]Mostowy RJ, Croucher NJ, De Maio N, Chewapreecha C, Salter SJ, Turner P, et al Pneumococcal Capsule Synthesis Locus cps as Evolutionary Hotspot with Potential to Generate Novel Serotypes by Recombination. Molecular Biology and Evolution. 2017; 34(10): 2537– 54. 10.1093/molbev/msx173 WOS:000411814800008. 28595308 PMC5850285 · DOI
  6. [6]McBride SM, Fischetti VA, LeBlanc DJ, Moellering RC, Gilmore MS. Genetic Diversity among Enterococcus faecalis. Plos One. 2007; 2(7). ARTN e582 10.1371/journal.pone.0000582 WOS:000207451900002. 17611618 PMC1899230 · DOI
  7. [7]Spinosa MR, Progida C, Tala A, Cogli L, Alifano P, Bucci C. The Neisseria meningitidis capsule is important for intracellular survival in human cells. Infect Immun. 2007; 75(7): 3594– 603. 10.1128/IAI.01945-06 WOS:000247707600041. 17470547 PMC1932921 · DOI
  8. [8]Zaragoza O, Chrisman CJ, Castelli MV, Frases S, Cuenca-Estrella M, Rodriguez-Tudela JL, et al Capsule enlargement in Cryptococcus neoformans confers resistance to oxidative stress suggesting a mechanism for intracellular survival. Cell Microbiol. 2008; 10(10): 2043– 57. 10.1111/j.1462-5822.2008.01186.x WOS:000259086900011. 18554313 PMC4405381 · DOI
  9. [9]Geisinger E, Isberg RR. Antibiotic modulation of capsular exopolysaccharide and virulence in Acinetobacter baumannii. PLoS Pathog. 2015; 11(2): e1004691 10.1371/journal.ppat.1004691 25679516 PMC4334535 · DOI
  10. [10]Llobet E, Tomas JM, Bengoechea JA. Capsule polysaccharide is a bacterial decoy for antimicrobial peptides. Microbiol-Sgm. 2008; 154: 3877– 86. 10.1099/mic.0.2008/022301-0 WOS:000261974700026. 19047754 · DOI
  11. [11]Campos MA, Vargas MA, Regueiro V, Llompart CM, Alberti S, Bengoechea JA. Capsule polysaccharide mediates bacterial resistance to antimicrobial peptides. Infect Immun. 2004; 72(12): 7107– 14. 10.1128/IAI.72.12.7107-7114.2004 WOS:000225453900040. 15557634 PMC529140 · DOI
  12. [12]Ophir T, Gutnick DL. A role for exopolysaccharides in the protection of microorganisms from desiccation. Appl Environ Microbiol. 1994; 60(2): 740– 5. 16349202 PMC201377
  13. [13]Roberts IS. The biochemistry and genetics of capsular polysaccharide production in bacteria. Annu Rev Microbiol. 1996; 50: 285– 315. 10.1146/annurev.micro.50.1.285. 8905082 · DOI
  14. [14]Rendueles O, Kaplan JB, Ghigo JM. Antibiofilm polysaccharides. Environ Microbiol. 2013; 15(2): 334– 46. 10.1111/j.1462-2920.2012.02810.x 22730907 PMC3502681 · DOI · Paper page
  15. [15]Rendueles O, Travier L, Latour-Lambert P, Fontaine T, Magnus J, Denamur E, et al Screening of Escherichia coli species biodiversity reveals new biofilm-associated antiadhesion polysaccharides. MBio. 2011; 2(3): e00043– 11. 10.1128/mBio.00043-11 21558434 PMC3101779 · DOI
  16. [16]Valle J, Da Re S, Henry N, Fontaine T, Balestrino D, Latour-Lambert P, et al Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci U S A. 2006; 103(33): 12558– 63. 10.1073/pnas.0605399103 16894146 PMC1567917 · DOI
  17. [17]Rendueles O, Garcia-Garcera M, Neron B, Touchon M, Rocha EPC. Abundance and co-occurrence of extracellular capsules increase environmental breadth: Implications for the emergence of pathogens. PLoS Pathog. 2017; 13(7): e1006525 10.1371/journal.ppat.1006525 28742161 PMC5542703 · DOI · Paper page
  18. [18]Jeon B, Muraoka W, Scupham A, Zhang Q. Roles of lipooligosaccharide and capsular polysaccharide in antimicrobial resistance and natural transformation of Campylobacter jejuni. J Antimicrob Chemother. 2009; 63(3): 462– 8. 10.1093/jac/dkn529 19147521 PMC2640156 · DOI
  19. [19]Ravin AW. Reciprocal capsular transformations of pneumococci. J Bacteriol. 1959; 77(3): 296– 309. 13641188 PMC290367
  20. [20]Schaffner TO, Hinds J, Gould KA, Wuthrich D, Bruggmann R, Kuffer M, et al A point mutation in cpsE renders Streptococcus pneumoniae nonencapsulated and enhances its growth, adherence and competence. BMC Microbiol. 2014; 14: 210 10.1186/s12866-014-0210-x 25163487 PMC4243769 · DOI
  21. [21]Yother J, McDaniel LS, Briles DE. Transformation of encapsulated Streptococcus pneumoniae. J Bacteriol. 1986; 168(3): 1463– 5. 3782044 PMC213662
  22. [22]Marks LR, Reddinger RM, Hakansson AP. High levels of genetic recombination during nasopharyngeal carriage and biofilm formation in Streptococcus pneumoniae. MBio. 2012; 3(5). 10.1128/mBio.00200-12 23015736 PMC3448161 · DOI
  23. [23]Chewapreecha C, Harris SR, Croucher NJ, Turner C, Marttinen P, Cheng L, et al Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet. 2014; 46(3): 305– 9. 10.1038/ng.2895 24509479 PMC3970364 · DOI
  24. [24]Chaguza C, Andam CP, Harris SR, Cornick JE, Yang M, Bricio-Moreno L, et al Recombination in Streptococcus pneumoniae Lineages Increase with Carriage Duration and Size of the Polysaccharide Capsule. MBio. 2016; 7(5): e01053– 16. 10.1128/mBio.01053-16 27677790 PMC5040112 · DOI
  25. [25]Ohshima Y, Schumacherperdreau F, Peters G, Pulverer G. The Role of Capsule as a Barrier to Bacteriophage Adsorption in an Encapsulated Staphylococcus-simulans Strain. Med Microbiol Immun. 1988; 177(4): 229– 33. WOS:A1988P095400006. 2971134
  26. [26]Scholl D, Merril C. The genome of bacteriophage K1F, a T7-like phage that has acquired the ability to replicate on K1 strains of Escherichia coli. J Bacteriol. 2005; 187(24): 8499– 503. 10.1128/JB.187.24.8499-8503.2005 16321955 PMC1317022 · DOI
  27. [27]Wilkinson BJ, Holmes KM. Staphylococcus aureus cell surface: capsule as a barrier to bacteriophage adsorption. Infect Immun. 1979; 23(2): 549– 52. 154475 PMC414199
  28. [28]Herr KL, Carey AM, Heckman TI, Chavez JL, Johnson CN, Harvey E, et al Exopolysaccharide production in Caulobacter crescentus: A resource allocation trade-off between protection and proliferation. PLoS One. 2018; 13(1): e0190371 10.1371/journal.pone.0190371 29293585 PMC5749776 · DOI
  29. [29]Hsieh PF, Lin HH, Lin TL, Chen YY, Wang JT. Two T7-like Bacteriophages, K5-2 and K5-4, Each Encodes Two Capsule Depolymerases: Isolation and Functional Characterization. Sci Rep. 2017; 7(1): 4624 10.1038/s41598-017-04644-2 28676686 PMC5496888 · DOI
  30. [30]Scholl D, Rogers S, Adhya S, Merril CR. Bacteriophage K1-5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. J Virol. 2001; 75(6): 2509– 15. 10.1128/JVI.75.6.2509-2515.2001 11222673 PMC115872 · DOI
  31. [31]Stuy JH. Plasmid transfer in Haemophilus influenzae. J Bacteriol. 1979; 139(2): 520– 9. 313393 PMC216899
  32. [32]McBride SM, Fischetti VA, LeBlanc DJ, Moellering RC, Gilmore MS. Genetic Diversity among Enterococcus faecalis. Plos One. 2007; 2(7): e582 ARTN e582 10.1371/journal.pone.0000582 WOS:000207451900002. 17611618 PMC1899230 · DOI
  33. [33]Mustapha MM, Marsh JW, Krauland MG, Fernandez JO, de Lemos APS, Hotopp JCD, et al Genomic Investigation Reveals Highly Conserved, Mosaic, Recombination Events Associated with Capsular Switching among Invasive Neisseria meningitidis Serogroup W Sequence Type (ST)-11 Strains. Genome Biology and Evolution. 2016; 8(6): 2065– 75. 10.1093/gbe/evw122 WOS:000386368200017. 27289093 PMC4943193 · DOI
  34. [34]Wyres KL, Gorrie C, Edwards DJ, Wertheim HFL, Hsu LY, Van Kinh N, et al Extensive Capsule Locus Variation and Large-Scale Genomic Recombination within the Klebsiella pneumoniae Clonal Group 258. Genome Biology and Evolution. 2015; 7(5): 1267– 79. 10.1093/gbe/evv062 WOS:000356228800007. 25861820 PMC4453057 · DOI
  35. [35]Csuros M. Ancestral Reconstruction by Asymmetric Wagner Parsimony over Continuous Characters and Squared Parsimony over Distributions. Lect N Bioinformat. 2008; 5267: 72– 86. WOS:000260884600006.
  36. [36]Johnston C, Martin B, Fichant G, Polard P, Claverys JP. Bacterial transformation: distribution, shared mechanisms and divergent control. Nat Rev Microbiol. 2014; 12(3): 181– 96. 10.1038/nrmicro3199. 24509783 · DOI
  37. [37]Barker D, Meade A, Pagel M. Constrained models of evolution lead to improved prediction of functional linkage from correlated gain and loss of genes. Bioinformatics. 2007; 23(1): 14– 20. 10.1093/bioinformatics/btl558. 17090580 · DOI
  38. [38]Green BD, Battisti L, Koehler TM, Thorne CB, Ivins BE. Demonstration of a capsule plasmid in Bacillus anthracis. Infect Immun. 1985; 49(2): 291– 7. 3926644 PMC262013
  39. [39]Brezillon C, Haustant M, Dupke S, Corre JP, Lander A, Franz T, et al Capsules, toxins and AtxA as virulence factors of emerging Bacillus cereus biovar anthracis. PLoS neglected tropical diseases. 2015; 9(4): e0003455 10.1371/journal.pntd.0003455 25830379 PMC4382292 · DOI
  40. [40]Sirard JC, Guidi-Rontani C, Fouet A, Mock M. Characterization of a plasmid region involved in Bacillus anthracis toxin production and pathogenesis. Int J Med Microbiol. 2000; 290(4–5): 313– 6. 10.1016/S1438-4221(00)80030-2. 11111904 · DOI
  41. [41]Smillie C, Garcillan-Barcia MP, Francia MV, Rocha EP, de la Cruz F. Mobility of plasmids. Microbiol Mol Biol Rev. 2010; 74(3): 434– 52. 10.1128/MMBR.00020-10 20805406 PMC2937521 · DOI
  42. [42]Guglielmini J, de la Cruz F, Rocha EP. Evolution of conjugation and type IV secretion systems. Mol Biol Evol. 2013; 30(2): 315– 31. 10.1093/molbev/mss221 22977114 PMC3548315 · DOI
  43. [43]Bueno SM, Santiviago CA, Murillo AA, Fuentes JA, Trombert AN, Rodas PI, et al Precise excision of the large pathogenicity island, SPI7, in Salmonella enterica serovar Typhi. J Bacteriol. 2004; 186(10): 3202– 13. 10.1128/JB.186.10.3202-3213.2004 15126483 PMC400632 · DOI
  44. [44]Jeltsch A. Maintenance of species identity and controlling speciation of bacteria: a new function for restriction/modification systems? Gene. 2003; 317(1–2): 13– 6. 10.1016/S0378-1119(03)00652-8 WOS:000186667000003. 14604787 · DOI
  45. [45]Hille F, Charpentier E. CRISPR-Cas: biology, mechanisms and relevance. Philos Trans R Soc Lond B Biol Sci. 2016; 371(1707). 10.1098/rstb.2015.0496 27672148 PMC5052741 · DOI
  46. [46]Gophna U, Kristensen DM, Wolf YI, Popa O, Drevet C, Koonin EV. No evidence of inhibition of horizontal gene transfer by CRISPR-Cas on evolutionary timescales. Isme Journal. 2015; 9(9): 2021– 7. 10.1038/ismej.2015.20 WOS:000360019500011. 25710183 PMC4542034 · DOI
  47. [47]Oliveira PH, Touchon M, Rocha EP. Regulation of genetic flux between bacteria by restriction-modification systems. Proc Natl Acad Sci U S A. 2016; 113(20): 5658– 63. 10.1073/pnas.1603257113 27140615 PMC4878467 · DOI · Paper page
  48. [48]Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol. 2010; 8(4): 251– 9. 10.1038/nrmicro2312. 20190823 · DOI · Paper page
  49. [49]Lopatkin AJ, Sysoeva TA, You L. Dissecting the effects of antibiotics on horizontal gene transfer: Analysis suggests a critical role of selection dynamics. Bioessays. 2016; 38(12): 1283– 92. 10.1002/bies.201600133. 27699821 PMC6541220 · DOI · Paper page
  50. [50]Pendleton JN, Gorman SP, Gilmore BF. Clinical relevance of the ESKAPE pathogens. Expert Rev Anti Infect Ther. 2013; 11(3): 297– 308. 10.1586/eri.13.12. 23458769 · DOI
  51. [51]Gibson MK, Forsberg KJ, Dantas G. Improved annotation of antibiotic resistance determinants reveals microbial resistomes cluster by ecology. ISME J. 2015; 9(1): 207– 16. 10.1038/ismej.2014.106 25003965 PMC4274418 · DOI
  52. [52]Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L, et al ARG-ANNOT, a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrob Agents Chemother. 2014; 58(1): 212– 20. 10.1128/AAC.01310-13 24145532 PMC3910750 · DOI · Paper page
  53. [53]Jia B, Raphenya AR, Alcock B, Waglechner N, Guo P, Tsang KK, et al CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 2017; 45(D1): D566– D73. 10.1093/nar/gkw1004 27789705 PMC5210516 · DOI
  54. [54]Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012; 67(11): 2640– 4. 10.1093/jac/dks261 22782487 PMC3468078 · DOI · Paper page
  55. [55]Arnold ML, Sapir Y, Martin NH. Genetic exchange and the origin of adaptations: prokaryotes to primates. Philos Trans R Soc Lond B Biol Sci. 2008; 363(1505): 2813– 20. 10.1098/rstb.2008.0021 18522920 PMC2606731 · DOI
  56. [56]Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature. 2000; 405(6784): 299– 304. 10.1038/35012500. 10830951 · DOI · Paper page
  57. [57]Manson JM, Hancock LE, Gilmore MS. Mechanism of chromosomal transfer of Enterococcus faecalis pathogenicity island, capsule, antimicrobial resistance, and other traits. Proc Natl Acad Sci U S A. 2010; 107(27): 12269– 74. 10.1073/pnas.1000139107 20566881 PMC2901427 · DOI · Paper page
  58. [58]Hilton T, Rosche T, Froelich B, Smith B, Oliver J. Capsular polysaccharide phase variation in Vibrio vulnificus. Appl Environ Microbiol. 2006; 72(11): 6986– 93. 10.1128/AEM.00544-06 16936057 PMC1636181 · DOI
  59. [59]Krinos CM, Coyne MJ, Weinacht KG, Tzianabos AO, Kasper DL, Comstock LE. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature. 2001; 414(6863): 555– 8. 10.1038/35107092. 11734857 · DOI
  60. [60]Brophy LN, Kroll JS, Ferguson DJP, Moxon ER. Capsulation Gene Loss and Rescue Mutations during the Cap+ to Cap- Transition in Haemophilus-Influenzae Type-B. Journal of General Microbiology. 1991; 137: 2571– 6. 10.1099/00221287-137-11-2571 WOS:A1991GR07500010. 1783904 · DOI
  61. [61]Lakkitjaroen N, Takamatsu D, Okura M, Sato M, Osaki M, Sekizaki T. Loss of capsule among Streptococcus suis isolates from porcine endocarditis and its biological significance. J Med Microbiol. 2011; 60(11): 1669– 76. 10.1099/jmm.0.034686–0 WOS:000296547900014. 21778266 · DOI
  62. [62]King JE, Aal Owaif HA, Jia J, Roberts IS. Phenotypic Heterogeneity in Expression of the K1 Polysaccharide Capsule of Uropathogenic Escherichia coli and Downregulation of the Capsule Genes during Growth in Urine. Infect Immun. 2015; 83(7): 2605– 13. 10.1128/IAI.00188-15 25870229 PMC4468546 · DOI
  63. [63]Gallie J, Libby E, Bertels F, Remigi P, Jendresen CB, Ferguson GC, et al Bistability in a metabolic network underpins the de novo evolution of colony switching in Pseudomonas fluorescens. PLoS Biol. 2015; 13(3): e1002109 10.1371/journal.pbio.1002109 25763575 PMC4357382 · DOI
  64. [64]Aminov RI. Horizontal gene exchange in environmental microbiota. Front Microbiol. 2011; 2: 158 10.3389/fmicb.2011.00158 21845185 PMC3145257 · DOI
  65. [65]Pando JM, Karlinsey JE, Lara JC, Libby SJ, Fang FC. The Rcs-Regulated Colanic Acid Capsule Maintains Membrane Potential in Salmonella enterica serovar Typhimurium. MBio. 2017; 8(3): e00808– 17. 10.1128/mBio.00808-17 28588134 PMC5461412 · DOI
  66. [66]Goerke C, Koller J, Wolz C. Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob Agents Chemother. 2006; 50(1): 171– 7. 10.1128/AAC.50.1.171-177.2006 16377683 PMC1346766 · DOI
  67. [67]Maiques E, Ubeda C, Campoy S, Salvador N, Lasa I, Novick RP, et al beta-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J Bacteriol. 2006; 188(7): 2726– 9. 10.1128/JB.188.7.2726-2729.2006 16547063 PMC1428414 · DOI
  68. [68]Stanczak-Mrozek KI, Laing KG, Lindsay JA. Resistance gene transfer: induction of transducing phage by sub-inhibitory concentrations of antimicrobials is not correlated to induction of lytic phage. J Antimicrob Chemother. 2017; 72(6): 1624– 31. 10.1093/jac/dkx056 28369562 PMC5437526 · DOI
  69. [69]Sailer FC, Meberg BM, Young KD. beta-Lactam induction of colanic acid gene expression in Escherichia coli. FEMS Microbiol Lett. 2003; 226(2): 245– 9. 10.1016/S0378-1097(03)00616-5. 14553918 · DOI
  70. [70]Dobson SRM, Kroll JS, Moxon ER. Insertion-Sequence Is1016 and Absence of Haemophilus Capsulation Genes in the Brazilian Purpuric Fever Clone of Haemophilus-Influenzae Biogroup Aegyptius. Infect Immun. 1992; 60(2): 618– 22. WOS:A1992HA56400044. 1309721 PMC257674
  71. [71]Salter SJ, Hinds J, Gould KA, Lambertsen L, Hanage WP, Antonio M, et al Variation at the capsule locus, cps, of mistyped and non-typable Streptococcus pneumoniae isolates. Microbiol-Sgm. 2012; 158: 1560– 9. 10.1099/mic.0.056580–0 WOS:000306500700018. PMC3541774 22403189 · DOI
  72. [72]Li G, Liang Z, Wang X, Yang Y, Shao Z, Li M, et al Addiction of Hypertransformable Pneumococcal Isolates to Natural Transformation for In Vivo Fitness and Virulence. Infect Immun. 2016; 84(6): 1887– 901. 10.1128/IAI.00097-16 27068094 PMC4907133 · DOI
  73. [73]Rowji P, Gromkova R, Koornhof H. Genetic transformation in encapsulated clinical isolates of Haemophilus influenzae type b. J Gen Microbiol. 1989; 135(10): 2775– 82. 10.1099/00221287-135-10-2775. 2632671 · DOI
  74. [74]Markowitz SM, Macrina FL, Phibbs PV Jr. R-factor inheritance and plasmid content in mucoid Pseudomonas aeruginosa. Infect Immun. 1978; 22(2): 530– 9. 103834 PMC422188
  75. [75]Cury J, Jove T, Touchon M, Neron B, Rocha EP. Identification and analysis of integrons and cassette arrays in bacterial genomes. Nucleic Acids Res. 2016; 44(10): 4539– 50. 10.1093/nar/gkw319 27130947 PMC4889954 · DOI
  76. [76]Touchon M, Cury J, Yoon EJ, Krizova L, Cerqueira GC, Murphy C, et al The genomic diversification of the whole Acinetobacter genus: origins, mechanisms, and consequences. Genome Biol Evol. 2014; 6(10): 2866– 82. 10.1093/gbe/evu225 25313016 PMC4224351 · DOI
  77. [77]Steinegger M, Soding J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol. 2017; 35(11): 1026– 8. 10.1038/nbt.3988. 29035372 · DOI · Paper page
  78. [78]Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4): 772– 80. 10.1093/molbev/mst010 23329690 PMC3603318 · DOI · Paper page
  79. [79]Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015; 32(1): 268– 74. 10.1093/molbev/msu300 25371430 PMC4271533 · DOI · Paper page
  80. [80]Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011; 27(4): 592– 3. 10.1093/bioinformatics/btq706 21169378 PMC3035803 · DOI
  81. [81]Didelot X, Wilson DJ. ClonalFrameML: Efficient Inference of Recombination in Whole Bacterial Genomes. Plos Comput Biol. 2015; 11(2): e1004041 ARTN e1004041 10.1371/journal.pcbi.1004041 WOS:000352081000015. 25675341 PMC4326465 · DOI
  82. [82]Didelot X, Falush D. Inference of bacterial microevolution using multilocus sequence data. Genetics. 2007; 175(3): 1251– 66. 10.1534/genetics.106.063305 17151252 PMC1840087 · DOI
  83. [83]Cadillo-Quiroz H, Didelot X, Held NL, Herrera A, Darling A, Reno ML, et al Patterns of gene flow define species of thermophilic Archaea. PLoS Biol. 2012; 10(2): e1001265 10.1371/journal.pbio.1001265 22363207 PMC3283564 · DOI
  84. [84]Didelot X, Bowden R, Street T, Golubchik T, Spencer C, McVean G, et al Recombination and population structure in Salmonella enterica. PLoS Genet. 2011; 7(7): e1002191 10.1371/journal.pgen.1002191 21829375 PMC3145606 · DOI
  85. [85]Vos M, Didelot X. A comparison of homologous recombination rates in bacteria and archaea. ISME J. 2009; 3(2): 199– 208. 10.1038/ismej.2008.93. 18830278 · DOI
  86. [86]Bruen TC, Philippe H, Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics. 2006; 172(4): 2665– 81. 10.1534/genetics.105.048975 16489234 PMC1456386 · DOI
  87. [87]Csuros M. Count: evolutionary analysis of phylogenetic profiles with parsimony and likelihood. Bioinformatics. 2010; 26(15): 1910– 2. 10.1093/bioinformatics/btq315. 20551134 · DOI
  88. [88]Lagesen K, Hallin P, Rodland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Research. 2007; 35(9): 3100– 8. 10.1093/nar/gkm160 WOS:000247350800027. 17452365 PMC1888812 · DOI
  89. [89]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. 10.1093/bioinformatics/btp348 19505945 PMC2712344 · DOI
  90. [90]Bernheim A, Calvo-Villamanan A, Basier C, Cui L, Rocha EPC, Touchon M, et al Inhibition of NHEJ repair by type II-A CRISPR-Cas systems in bacteria. Nat Commun. 2017; 8(1): 2094 10.1038/s41467-017-02350-1. 29234047 PMC5727150 · DOI
  91. [91]Filipski A, Murillo O, Freydenzon A, Tamura K, Kumar S. Prospects for Building Large Timetrees Using Molecular Data with Incomplete Gene Coverage among Species. Molecular Biology and Evolution. 2014; 31(9): 2542– 50. 10.1093/molbev/msu200 WOS:000343401100024. 24974376 PMC4137717 · DOI
  92. [92]Price MN, Dehal PS, Arkin AP. FastTree: Computing Large Minimum Evolution Trees with Profiles instead of a Distance Matrix. Molecular Biology and Evolution. 2009; 26(7): 1641– 50. 10.1093/molbev/msp077 WOS:000266966200020. 19377059 PMC2693737 · DOI · Paper page
  93. [93]Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol. 2012; 3(2): 217– 23. 10.1111/j.2041-210X.2011.00169.x WOS:000302538500001. · DOI
  94. [94]Ives AR, Garland T. Phylogenetic Logistic Regression for Binary Dependent Variables. Systematic Biology. 2010; 59(1): 9– 26. 10.1093/sysbio/syp074 WOS:000272689500002. 20525617 · DOI
  95. [95]Paradis E, Claude J, Strimmer K. APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics. 2004; 20(2): 289– 90.. 14734327
  96. [96]Abby SS, Neron B, Menager H, Touchon M, Rocha EP. MacSyFinder: a program to mine genomes for molecular systems with an application to CRISPR-Cas systems. PLoS One. 2014; 9(10): e110726 10.1371/journal.pone.0110726 25330359 PMC4201578 · DOI

Cited by

Sorted by citations

Authors
Rendueles, O., de Sousa, J. A. M., Bernheim, A., Touchon, M., & Rocha, E. P. C.
Affiliations
Centre National de la Recherche Scientifique (FR)
Corresponding author
Rendueles, Olaya
Venue
PLOS Genetics
Published
2018-12-21
Volume
14
Issue
12
Pages
e1007862
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
OpenAlex
W2905633810
Cited by
41
References
0
Citations by year
2026: 4 · 2025: 3 · 2024: 6 · 2023: 6 · 2022: 4 · 2021: 7 · 2020: 6 · 2019: 5
FWCI
2.72
Type
journal article
Language
en
Open access
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
bacterial capsule, genetic exchange, horizontal gene transfer, homologous recombination, pan-genome, plasmids, prophages, integrons, transposase, conjugative elements, antibiotic resistance genes, efflux pumps, nosocomial pathogens, bacterial colonization, core genome
MeSH terms
Bacteria, Phylogeny, Species Specificity, DNA Restriction-Modification Enzymes, Bacterial Capsules, Genome, Bacterial, Interspersed Repetitive Sequences, Gene Transfer, Horizontal, Drug Resistance, Bacterial, Homologous Recombination

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