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Clonally Evolving Pathogenic Bacteria

  • Sofia Hauck
  • Martin C. J. Maiden
Chapter
Part of the Grand Challenges in Biology and Biotechnology book series (GCBB)

Abstract

Unlike those of animals and plants, sexual processes in bacteria are not linked to reproduction per se and are a consequence of horizontal (sometimes called lateral) gene transfer (HGT). This is the acquisition of genetic material from a nonparental source and its incorporation into the genome, usually by recombination. The relative and absolute rates of HGT in different bacteria vary greatly, and this has a major influence on population diversity, structure and evolution. Rates of HGT are influenced by both mechanistic and ecological considerations, and when HGT is absent or very rare, bacterial populations become completely clonal. In such populations, evolution occurs solely by the accumulation of mutations, accompanied by diversity reduction events such as periodic selection and/or stochastic bottlenecks, which can result in hitchhiking events that fix mutations, whether beneficial, deleterious or neutral in their effect on fitness. The net effect is the establishment of distinct lineages within the population, which are characterized by low genetic diversity accompanied by the relaxation of purifying selection and an enhancement of the effects of genetic drift. The best examples of such bacteria are well-known obligate pathogens that affect humans, including Mycobacterium tuberculosis, Mycobacterium leprae, Yersinia pestis, Bacillus anthracis, Salmonella enterica serovar Typhi and Bordetella pertussis. Each of these pathogens has evolved from a more diverse parental population as a result of a shift in niche from a free-living organism to an obligate parasite. In some cases, this was caused or accompanied by a HGT event, but ultimately the process has led to reproductive isolation: the inhibition of further HGT with the parental population, the wider bacterial community, and even among members of the population itself. While this reproductive isolation may have promoted specialization and eventually speciation, it can also result in loss of fitness, as a consequence of the accumulation of deleterious or mildly deleterious mutations, a process known as Muller’s ratchet. Since their emergence, the evolution of these organisms has been further influenced by ecological factors resulting from changes in human behaviour, including increased population numbers and density and the use of antibiotics.

References

  1. Achtman M (2008) Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62:53–70.  https://doi.org/10.1146/annurev.micro.62.081307.162832 CrossRefPubMedGoogle Scholar
  2. Achtman M (2012) Insights from genomic comparisons of genetically monomorphic bacterial pathogens. 367:860–867.  https://doi.org/10.1098/rstb.2011.0303 CrossRefGoogle Scholar
  3. Achtman M, Wagner M (2008) Microbial diversity and the genetic nature of microbial species. Nat Rev Microbiol 6:431–440.  https://doi.org/10.1038/nrmicro1872 CrossRefPubMedGoogle Scholar
  4. Avise JC (2015) Evolutionary perspectives on clonal reproduction in vertebrate animals. Proc Natl Acad Sci U S A 112:8867–8873.  https://doi.org/10.1073/pnas.1501820112 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Ayyadurai S, Houhamdi L, Lepidi H et al (2008) Long-term persistence of virulent Yersinia pestis in soil. Microbiol Immunol 154:2865–2871.  https://doi.org/10.1099/mic.0.2007/016154-0 CrossRefGoogle Scholar
  6. Bapteste E, Boucher Y (2009) Epistemological impacts of horizontal gene transfer on classification in microbiology. Methods Mol Biol 532:55–72.  https://doi.org/10.1007/978-1-60327-853-9_4 CrossRefPubMedGoogle Scholar
  7. Bart MJ, Harris SR, Advani A et al (2014) Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. MBio 5:e01074–e01074–14.  https://doi.org/10.1128/mBio.01074-14 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bergstrom CT, McElhany P, Real LA (1999) Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proc Natl Acad Sci U S A 96:5095–5100CrossRefGoogle Scholar
  9. Bos KI, Schuenemann VJ, Golding GB et al (2011) A draft genome of Yersinia pestis from victims of the Black Death. Nature 478:506–510.  https://doi.org/10.1038/nature10549 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Cao Q, Didelot X, Wu Z et al (2015) Progressive genomic convergence of two Helicobacter pylori strains during mixed infection of a patient with chronic gastritis. Gut 64:554–561.  https://doi.org/10.1136/gutjnl-2014-307345 CrossRefPubMedGoogle Scholar
  11. Cohan FM (1994) Genetic exchange and evolutionary divergence in prokaryotes. Trends Ecol Evol 9:175–180.  https://doi.org/10.1016/0169-5347(94)90081-7 CrossRefPubMedGoogle Scholar
  12. Cohan FM (2002) Sexual isolation and speciation in bacteria. Genetica 116:359–370.  https://doi.org/10.1023/A:1021232409545 CrossRefPubMedGoogle Scholar
  13. Cole ST, Eiglmeier K, Parkhill J et al (2001) Massive gene decay in the leprosy bacillus. Nature 409:1007–1011.  https://doi.org/10.1038/35059006 CrossRefPubMedGoogle Scholar
  14. Comas I, Coscolla M, Luo T et al (2013) Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 45:1176–1182.  https://doi.org/10.1038/ng.2744 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Coscolla M, Gagneux S (2014) Consequences of genomic diversity in Mycobacterium tuberculosis. Semin Immunol 26:431–444.  https://doi.org/10.1016/j.smim.2014.09.012 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Croucher NJ, Mostowy R, Wymant C et al (2016) Horizontal DNA transfer mechanisms of bacteria as weapons of intragenomic conflict. PLoS Biol 14:e1002394.  https://doi.org/10.1371/journal.pbio.1002394 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cummings CA, Brinig MM, Lepp PW (2004) Bordetella species are distinguished by patterns of substantial gene loss and host adaptation. J Bacteriol.  https://doi.org/10.1128/JB.186.5.1484
  18. de Gouw D, Diavatopoulos D, Heuvelman K et al (2014) Differentially expressed genes in Bordetella pertussis strains belonging to a lineage which recently spread globally. PLoS One 9:e84523.  https://doi.org/10.1371/journal.pone.0084523 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Diavatopoulos DA, Cummings CA, Schouls LM, Brinig MM, Relman DA, Mooi FR (2005) Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog 1(4):e45CrossRefGoogle Scholar
  20. Didelot X, Bowden R, Street T et al (2011) Recombination and population structure in Salmonella enterica. PLoS Genet 7:e1002191–e1002191.  https://doi.org/10.1371/journal.pgen.1002191 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Didelot X, Pang B, Zhou Z et al (2015) The role of China in the global spread of the current cholera pandemic. PLoS Genet 11:e1005072.  https://doi.org/10.1371/journal.pgen.1005072 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Djelouadji Z, Raoult D, Drancourt M (2011) Palaeogenomics of Mycobacterium tuberculosis: epidemic bursts with a degrading genome. Lancet Infect Dis 11:641–650.  https://doi.org/10.1016/S1473-3099(11)70093-7 CrossRefPubMedGoogle Scholar
  23. Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413PubMedPubMedCentralGoogle Scholar
  24. Feil EJ, Spratt BG (2001) Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol 55:561–590.  https://doi.org/10.1146/annurev.micro.55.1.561 CrossRefPubMedGoogle Scholar
  25. Ford CB, Lin PL, Chase MR et al (2011) Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 43:482–486.  https://doi.org/10.1038/ng.811 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gage KL, Kosoy MY (2005) Natural history of plague: perspectives from more than a century of research. Annu Rev Entomol 50:505–528.  https://doi.org/10.1146/annurev.ento.50.071803.130337 CrossRefPubMedGoogle Scholar
  27. Galan JE (2016) Typhoid toxin provides a window into typhoid fever and the biology of Salmonella typhi. Proc Natl Acad Sci U S A 113:6338–6344.  https://doi.org/10.1073/pnas.1606335113 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Ghodbane R, Mba Medie F, Lepidi H et al (2014) Long-term survival of tuberculosis complex mycobacteria in soil. Microbiol Rev 160:496–501.  https://doi.org/10.1099/mic.0.073379-0 CrossRefGoogle Scholar
  29. Gordo I, Charlesworth B (2000) The degeneration of asexual haploid populations and the speed of Muller’s ratchet. Genetics 154:1379–1387.  https://doi.org/10.1016/S0960-9822(02)00448-7 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gross R, Keidel K, Schmitt K (2010) Resemblance and divergence: the “new” members of the genus Bordetella. Med Microbiol Immunol 199:155–163.  https://doi.org/10.1007/s00430-010-0148-z CrossRefPubMedGoogle Scholar
  31. Guiso N (2014) Bordetella pertussis: why is it still circulating? J Infect 68(Suppl 1):S119–S124.  https://doi.org/10.1016/j.jinf.2013.09.022 CrossRefPubMedGoogle Scholar
  32. Hanage WP, Fraser C, Spratt BG (2006a) The impact of homologous recombination on the generation of diversity in bacteria. J Theor Biol 239:210–219.  https://doi.org/10.1016/j.jtbi.2005.08.035 CrossRefPubMedGoogle Scholar
  33. Hanage WP, Fraser C, Spratt BG (2006b) Sequences, sequence clusters and bacterial species. Philos Trans R Soc B 361:1917–1927.  https://doi.org/10.1098/rstb.2006.1917 CrossRefGoogle Scholar
  34. Hanekom M, Gey Van Pittius NC, McEvoy C et al (2011) Mycobacterium tuberculosis Beijing genotype: a template for success. Tuberculosis 91:510–523.  https://doi.org/10.1016/j.tube.2011.07.005 CrossRefPubMedGoogle Scholar
  35. Hershberg R, Lipatov M, Small PM et al (2008) High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 6:e311.  https://doi.org/10.1371/journal.pbio.0060311 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Holt KE, Parkhill J, Mazzoni CJ et al (2008) High-throughput sequencing provides insights into genome variation and evolution in Salmonella typhi. Nat Genet 40:987–993.  https://doi.org/10.1038/ng.195 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Holt KE, Teo YY, Li H et al (2009) Detecting SNPs and estimating allele frequencies in clonal bacterial populations by sequencing pooled DNA. Vaccine 25:2074–2075.  https://doi.org/10.1093/bioinformatics/btp344 CrossRefGoogle Scholar
  38. Huttenhower C, Gevers D, Knight R et al (2012) Structure, function and diversity of the healthy human microbiome. Nature 486:207–214.  https://doi.org/10.1038/nature11234 CrossRefGoogle Scholar
  39. Kay GL, Sergeant MJ, Zhou Z et al (2015) Eighteenth-century genomes show that mixed infections were common at time of peak tuberculosis in Europe. Nat Commun 6:6717.  https://doi.org/10.1038/ncomms7717 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Keim P, Gruendike JM, Klevytska AM et al (2009) The genome and variation of Bacillus anthracis. Mol Aspects Med 30:397–405.  https://doi.org/10.1016/j.mam.2009.08.005 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kingsley RA, Msefula CL, Thomson NR et al (2009) Epidemic multiple drug resistant Salmonella typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 19:2279–2287.  https://doi.org/10.1101/gr.091017.109 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kohl TA, Diel R, Harmsen D et al (2014) Whole genome based Mycobacterium tuberculosis surveillance: a standardized, portable and expandable approach. J Clin Microbiol 52:2479–2486.  https://doi.org/10.1128/JCM.00567-14 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kolstø A-B, Tourasse NJ, Økstad OA (2009) What sets Bacillus anthracis apart from other Bacillus species? Annu Rev Microbiol 63:451–476.  https://doi.org/10.1146/annurev.micro.091208.073255 CrossRefPubMedGoogle Scholar
  44. Lan R, Reeves PR (2001) When does a clone deserve a name? A perspective on bacterial species based on population genetics. Trends Microbiol 9:419–424CrossRefGoogle Scholar
  45. Lehtonen J, Jennions MD, Kokko H (2012) The many costs of sex. Trends Ecol Evol 27:172–178.  https://doi.org/10.1016/j.tree.2011.09.016 CrossRefPubMedGoogle Scholar
  46. Levin BR (1981) Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99:1–23PubMedPubMedCentralGoogle Scholar
  47. Maiden MCJ, Bygraves JA, Feil E et al (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95:3140–3145.  https://doi.org/10.1073/pnas.95.6.3140 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Maiden MCJ, van Rensburg MJJ, Bray JE et al (2013) MLST revisited: the gene-by-gene approach to bacterial genomics. Nat Rev Microbiol 11:728–736.  https://doi.org/10.1038/nrmicro3093 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Maynard Smith J, Smith NH, O'Rourke M, Spratt BG (1993) How clonal are bacteria? Proc Natl Acad Sci U S A 90:4384–4388.  https://doi.org/10.1902/jop.2011.110063 CrossRefGoogle Scholar
  50. Merker M, Blin C, Mona S et al (2015) Evolutionary history and global spread of the Mycobacterium tuberculosis Beijing lineage. Nat Genet 47:242–249.  https://doi.org/10.1038/ng.3195 CrossRefPubMedGoogle Scholar
  51. Michod RE, Bernstein H, Nedelcu AM (2008) Adaptive value of sex in microbial pathogens. Infect Genet Evol 8:267–285.  https://doi.org/10.1016/j.meegid.2008.01.002 CrossRefPubMedGoogle Scholar
  52. Moffatt CRM, Greig A, Valcanis M et al (2016) A large outbreak of Campylobacter jejuni infection in a university college caused by chicken liver pâté, Australia, 2013. Epidemiol Infect 144:2971–2978.  https://doi.org/10.1017/S0950268816001187 CrossRefPubMedGoogle Scholar
  53. Mooi F (2010) Bordetella pertussis and vaccination: the persistence of a genetically monomorphic pathogen. Infect Genet Evol 10:36–49.  https://doi.org/10.1016/j.meegid.2009.10.007 CrossRefPubMedGoogle Scholar
  54. Moran NA, Plague GR (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14:627–633.  https://doi.org/10.1016/j.gde.2004.09.003 CrossRefPubMedGoogle Scholar
  55. Moran NA, Wernegreen JJ (2000) Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol 15:321–326CrossRefGoogle Scholar
  56. Moreno-Gamez S, Hilla AL, Rosenbloom DIS et al (2015) Imperfect drug penetration leads to spatial monotherapy and rapid evolution of multidrug resistance. Proc Natl Acad Sci U S A 112:E2874–E2883.  https://doi.org/10.1073/pnas.1424184112 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Namouchi A, Didelot X, Schöck U et al (2012) After the bottleneck: Genome-wide diversification of the Mycobacterium tuberculosis complex by mutation, recombination, and natural selection. Genome Res 22:721–734.  https://doi.org/10.1101/gr.129544.111 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218.  https://doi.org/10.1146/annurev.genet.39.073003.112420 CrossRefPubMedGoogle Scholar
  59. Niemann S, Merker M, Kohl T, Supply P (2016) Impact of genetic diversity on the biology of Mycobacterium tuberculosis complex strains. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.TBTB2-0022-2016
  60. Ohta T (1992) The nearly neutral theory of molecular evolution. Annu Rev Ecol Syst 23:263–286.  https://doi.org/10.2307/2097289 CrossRefGoogle Scholar
  61. Ohta T (2011) Near-neutrality, robustness, and epigenetics. Genome Biol Evol 3:1034–1038.  https://doi.org/10.1093/gbe/evr012 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Okinaka R, Pearson T, Keim P (2006) Anthrax, but not Bacillus anthracis? PLoS Pathog 2:e122CrossRefGoogle Scholar
  63. Orsi RH, Bowen BM, Wiedmann M (2010) Homopolymeric tracts represent a general regulatory mechanism in prokaryotes. BMC Genomics 11(1):102CrossRefGoogle Scholar
  64. Park J, Zhang Y, Buboltz AM et al (2012) Comparative genomics of the classical Bordetella subspecies: the evolution and exchange of virulence-associated diversity amongst closely related pathogens. BMC Genomics 13:545–545.  https://doi.org/10.1186/1471-2164-13-545 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Parkhill J, Sebaihia M, Preston A et al (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35:32–40.  https://doi.org/10.1038/ng1227 CrossRefPubMedGoogle Scholar
  66. Planet PJ, Narechania A, Chen L et al (2017) Architecture of a Species: phylogenomics of Staphylococcus aureus. Trends Microbiol 25:153–166.  https://doi.org/10.1016/j.tim.2016.09.009 CrossRefPubMedGoogle Scholar
  67. Polz MF, Alm EJ, Hanage WP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet 29:170–175.  https://doi.org/10.1016/j.tig.2012.12.006 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Rasko DA, Worsham PL, Abshire TG et al (2011) Bacillus anthracis comparative genome analysis in support of the Amerithrax investigation. Proc Natl Acad Sci U S A 108:5027–5032.  https://doi.org/10.1073/pnas.1016657108 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Rasmussen S, Allentoft ME, Nielsen K et al (2015) Early divergent strains of Yersinia pestis in Eurasia 5,000 years ago. Cell 163:571–582.  https://doi.org/10.1016/j.cell.2015.10.009 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Redfield RJ, Findlay WA, Bosse J et al (2006) Evolution of competence and DNA uptake specificity in the Pasteurellaceae. BMC Evol Biol 6:82.  https://doi.org/10.1186/1471-2148-6-82 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Reiling N, Homolka S, Walter K et al (2013) Clade-specific virulence patterns of Mycobacterium tuberculosis complex strains in human primary macrophages and aerogenically infected mice. MBio 4:e00250–e00213.  https://doi.org/10.1128/mBio.00250-13 CrossRefPubMedPubMedCentralGoogle Scholar
  72. Rocha E, Maynard Smith J, Hurst LD et al (2006) Comparisons of dN/dS are time dependent for closely related bacterial genomes. J Theor Biol 239:226–235.  https://doi.org/10.1016/j.jtbi.2005.08.037 CrossRefPubMedGoogle Scholar
  73. Roumagnac P, Weill F-X, Dolecek C et al (2006) Evolutionary history of Salmonella typhi. Science 314:1301–1304.  https://doi.org/10.1126/science.1134933 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Shapiro BJ (2016) How clonal are bacteria over time? Curr Opin Microbiol 31:116–123.  https://doi.org/10.1016/j.mib.2016.03.013 CrossRefPubMedGoogle Scholar
  75. Smith NH, Gordon SV, de la Rua-Domenech R et al (2006) Bottlenecks and broomsticks: the molecular evolution of Mycobacterium bovis. Nat Rev Microbiol 4:670–681.  https://doi.org/10.1038/nrmicro1472 CrossRefPubMedGoogle Scholar
  76. Soares P, Alshamali F, Pereira JB et al (2012) The expansion of mtDNA Haplogroup L3 within and out of Africa. Mol Biol Evol 29:915–927.  https://doi.org/10.1093/molbev/msr245 CrossRefPubMedGoogle Scholar
  77. Spratt BG, Maiden MCJ (1999) Bacterial population genetics, evolution and epidemiology. Philos Trans R Soc B 354:701–710.  https://doi.org/10.1098/rstb.1999.0423 CrossRefGoogle Scholar
  78. Stackebrandt E, Frederiksen W, Garrity GM et al (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047.  https://doi.org/10.1099/00207713-52-3-1043 CrossRefPubMedGoogle Scholar
  79. Suerbaum S, Smith JM, Bapumia K et al (1998) Free recombination within Helicobacter pylori. Proc Natl Acad Sci U S A 95:12619–12624CrossRefGoogle Scholar
  80. Tibayrenc M, Ayala FJ (2002) The clonal theory of parasitic protozoa: 12 years on. Trends Parasitol 18:405–410CrossRefGoogle Scholar
  81. Tibayrenc M, Ayala FJ (2012) Reproductive clonality of pathogens: a perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. Proc Natl Acad Sci U S A 109:E3305–E3313.  https://doi.org/10.1073/pnas.1212452109 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Tibayrenc M, Ayala FJ (2015) How clonal are Neisseria species? The epidemic clonality model revisited. Proc Natl Acad Sci U S A 112:8909–8913.  https://doi.org/10.1073/pnas.1502900112 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Tibayrenc M, Ayala FJ (2016) Is predominant clonal evolution a common evolutionary adaptation to parasitism in pathogenic parasitic protozoa, fungi, bacteria, and viruses? Adv Parasitol 97:243–325CrossRefGoogle Scholar
  84. Turner KME, Feil EJ (2007) The secret life of the multilocus sequence type. Int J Antimicrob Agents 29:129–135CrossRefGoogle Scholar
  85. van der Veen S, Tang CM (2015) The BER necessities: the repair of DNA damage in human-adapted bacterial pathogens. Nat Rev Microbiol 13:83–94.  https://doi.org/10.1038/nrmicro3391 CrossRefPubMedGoogle Scholar
  86. Votintseva AA, Miller RR, Fung R et al (2014) Multiple-strain colonization in nasal carriers of Staphylococcus aureus. J Clin Microbiol 52:1192–1200.  https://doi.org/10.1128/JCM.03254-13 CrossRefPubMedPubMedCentralGoogle Scholar
  87. Vultos Dos T, Mestre O, Rauzier J et al (2008) Evolution and diversity of clonal bacteria: the paradigm of Mycobacterium tuberculosis. PLoS One 3:e1538–e1538.  https://doi.org/10.1371/journal.pone.0001538 CrossRefGoogle Scholar
  88. Wiedenbeck J, Cohan FM (2011) Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev 35:957–976.  https://doi.org/10.1111/j.1574-6976.2011.00292.x CrossRefPubMedGoogle Scholar
  89. Woodford N, Ellington MJ (2007) The emergence of antibiotic resistance by mutation. Clin Microbiol Infect 13:5–18.  https://doi.org/10.1111/j.1469-0691.2006.01492.x CrossRefPubMedGoogle Scholar
  90. Yahara K, Didelot X, Jolley KA et al (2016) The landscape of realized homologous recombination in pathogenic bacteria. Mol Biol Evol 33:456–471.  https://doi.org/10.1093/molbev/msv237 CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of OxfordOxfordUK

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