1887

Abstract

is an important global pathogen that causes bacterial pneumonia, sepsis and meningitis. Beta-lactam antibiotics are the first-line treatment for pneumococcal disease, however, their effectiveness is hampered by beta-lactam resistance facilitated by horizontal genetic transfer (HGT) with closely related species. Although interspecies HGT is known to occur among the species of the genus , the rates and effects of HGT between and its close relatives involving the penicillin binding protein () genes remain poorly understood. Here we applied the fastGEAR tool to investigate interspecies HGT in genes using a global collection of whole-genome sequences of , and . With these data, we established that pneumococcal serotypes 6A, 13, 14, 16F, 19A, 19F, 23F and 35B were the highest-ranking serotypes with acquired fragments. was a more frequent pneumococcal donor of fragments and a source of higher nucleotide diversity when compared with . Pneumococci that acquired fragments were associated with a higher minimum inhibitory concentration (MIC) for penicillin compared with pneumococci without acquired fragments. Together these data indicate that contributes to reduced β-lactam susceptibility among commonly carried pneumococcal serotypes that are associated with long carriage duration and high recombination frequencies. As pneumococcal vaccine programmes mature, placing increasing pressure on the pneumococcal population structure, it will be important to monitor the influence of antimicrobial resistance HGT from commensal streptococci such as .

Funding
This study was supported by the:
  • Bill and Melinda Gates Foundation (Award OPP1034556)
    • Principle Award Recipient: StephenD. Bentley
  • National Institute for Health Research (Award 16/136/46)
    • Principle Award Recipient: RobertS. Heyderman
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
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2021-09-22
2024-03-29
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References

  1. O’Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 2009; 374:893–902 [View Article] [PubMed]
    [Google Scholar]
  2. O’Brien KL, Baggett HC, Brooks WA, Feikin DR, Hammitt LL et al. Causes of severe pneumonia requiring hospital admission in children without HIV infection from Africa and Asia: the PERCH multi-country case-control study. Lancet 2019; 394:757–779 [View Article] [PubMed]
    [Google Scholar]
  3. Wahl B, O’Brien KL, Greenbaum A, Majumder A, Liu L et al. Burden of Streptococcus pneumoniae and Haemophilus influenzae type b disease in children in the era of conjugate vaccines: global, regional, and national estimates for 2000-15. Lancet Glob Health 2018; 6:57e744 [View Article] [PubMed]
    [Google Scholar]
  4. Cohen C, von MC, de GL, Lengana S, Meiring S et al. Effectiveness of the 13-valent pneumococcal conjugate vaccine against invasive pneumococcal disease in South African children: a case-control study. The Lancet Global Health 2017; 5:e359-69 [View Article]
    [Google Scholar]
  5. Turner P, Leab P, Ly S, Sao S, Miliya T et al. Impact of 13-valent pneumococcal conjugate vaccine on colonization and invasive disease in Cambodian children. Clin Infect Dis 2020; 70:1580–1588 [View Article] [PubMed]
    [Google Scholar]
  6. Klugman KP, Black S. Impact of existing vaccines in reducing antibiotic resistance: primary and secondary effects. Proc Natl Acad Sci U S A 2018; 115:12896–12901 [View Article] [PubMed]
    [Google Scholar]
  7. Kyaw MH, Lynfield R, Schaffner W, Craig AS, Hadler J et al. Effect of introduction of the pneumococcal conjugate vaccine on drug-resistant Streptococcus pneumoniae. N Engl J Med 2006; 354:1455–1463 [View Article] [PubMed]
    [Google Scholar]
  8. Olarte L, Kaplan SL, Barson WJ, Romero JR, Lin PL et al. Emergence of multidrug-resistant pneumococcal serotype 35B among children in the United States. J Clin Microbiol 2017; 55:724–734 [View Article] [PubMed]
    [Google Scholar]
  9. Ladhani SN, Collins S, Djennad A, Sheppard CL, Borrow R et al. Rapid increase in non-vaccine serotypes causing invasive pneumococcal disease in England and Wales, 2000–17: a prospective national observational cohort study. Lancet Infect Dis 2018; 18:441–451 [View Article] [PubMed]
    [Google Scholar]
  10. Swarthout TD, Fronterre C, Lourenço J, Obolski U, Gori A et al. High residual carriage of vaccine-serotype Streptococcus pneumoniae after introduction of pneumococcal conjugate vaccine in Malawi. Nat Commun 2020; 11:2222 [View Article] [PubMed]
    [Google Scholar]
  11. Manenzhe RI, Moodley C, Abdulgader SM, Robberts FJL, Zar HJ et al. Nasopharyngeal carriage of antimicrobial-resistant pneumococci in an intensively sampled South African birth cohort. Front Microbiol 2019; 10:610 [View Article] [PubMed]
    [Google Scholar]
  12. Croucher NJ, Harris SR, Fraser C, Quail MA, Burton J et al. Rapid pneumococcal evolution in response to clinical interventions. Science 2011; 331:430–434 [View Article] [PubMed]
    [Google Scholar]
  13. Croucher NJ, Chewapreecha C, Hanage WP, Harris SR, McGee L et al. Evidence for soft selective sweeps in the evolution of pneumococcal multidrug resistance and vaccine escape. Genome Biol Evol 2014; 6:1589–1602 [View Article] [PubMed]
    [Google Scholar]
  14. Croucher NJ, Kagedan L, Thompson CM, Parkhill J, Bentley SD et al. Selective and genetic constraints on pneumococcal serotype switching. PLoS Genet 2015; 11:e1005095 [View Article] [PubMed]
    [Google Scholar]
  15. Chaguza C, Cornick JE, Andam CP, Gladstone RA, Alaerts M et al. Population genetic structure, antibiotic resistance, capsule switching and evolution of invasive pneumococci before conjugate vaccination in Malawi. Vaccine 2017; 35:4594–4602 [View Article] [PubMed]
    [Google Scholar]
  16. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018; 18:318–327 [View Article] [PubMed]
    [Google Scholar]
  17. Chochua S, Metcalf BJ, Li Z, Walker H, Tran T et al. Invasive serotype 35B pneumococci including an expanding serotype switch lineage, United States, 2015–2016. Emerg Infect Dis 2017; 23:922–930 [View Article] [PubMed]
    [Google Scholar]
  18. Andam CP, Mitchell PK, Callendrello A, Chang Q, Corander J et al. Genomic epidemiology of penicillin-nonsusceptible pneumococci with nonvaccine serotypes causing invasive disease in the United States. J Clin Microbiol 2017; 55:1104–1115 [View Article] [PubMed]
    [Google Scholar]
  19. Madhi SA, Nzenze SA, Nunes MC, Chinyanganya L, Van Niekerk N et al. Residual colonization by vaccine serotypes in rural South Africa four years following initiation of pneumococcal conjugate vaccine immunization. Expert Rev Vaccines 2020; 19:383–393 [View Article] [PubMed]
    [Google Scholar]
  20. Usuf E, Bottomley C, Adegbola RA, Hall A. Pneumococcal carriage in Sub-Saharan Africa—A systematic review. PLoS One 2014; 9:e85001 [View Article] [PubMed]
    [Google Scholar]
  21. Kandasamy R, Voysey M, Collins S, Berbers G, Robinson H et al. Persistent circulation of vaccine serotypes and serotype replacement after 5 years of infant immunization with 13-valent pneumococcal conjugate vaccine in the United Kingdom. J Infect Dis 2020; 221:1361–1370 [View Article] [PubMed]
    [Google Scholar]
  22. McGee L, McDougal L, Zhou J, Spratt BG, Tenover FC et al. Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the pneumococcal molecular epidemiology network. J Clin Microbiol 2001; 39:2565–2571 [View Article] [PubMed]
    [Google Scholar]
  23. Ho P-L, Chiu SS, Law PY, Chan EL, Lai EL et al. Increase in the nasopharyngeal carriage of non-vaccine serogroup 15 Streptococcus pneumoniae after introduction of children pneumococcal conjugate vaccination in Hong Kong. Diagn Microbiol Infect Dis 2015; 81:145–148 [View Article] [PubMed]
    [Google Scholar]
  24. Nakano S, Fujisawa T, Ito Y, Chang B, Matsumura Y et al. Spread of meropenem-resistant Streptococcus pneumoniae serotype 15A-ST63 clone in Japan, 2012–2014. Emerg Infect Dis 2018; 24:275–283 [View Article] [PubMed]
    [Google Scholar]
  25. Golden AR, Adam HJ, Gilmour MW, Baxter MR, Martin I et al. Assessment of multidrug resistance, clonality and virulence in non-PCV-13 Streptococcus pneumoniae serotypes in Canada, 2011–13. J Antimicrob Chemother 2015; 70:1960–1964 [View Article] [PubMed]
    [Google Scholar]
  26. Liñares J, Ardanuy C, Pallares R, Fenoll A. Changes in antimicrobial resistance, serotypes and genotypes in Streptococcus pneumoniae over a 30-year period. Clin Microbiol Infect 2010; 16:402–410 [View Article] [PubMed]
    [Google Scholar]
  27. Amoroso A, Demares D, Mollerach M, Gutkind G, Coyette J. All detectable high-molecular-mass penicillin-binding proteins are modified in a high-level beta-lactam-resistant clinical isolate of Streptococcus mitis. Antimicrob Agents Chemother 2001; 45:2075–2081 [View Article] [PubMed]
    [Google Scholar]
  28. Hakenbeck R, Brückner R, Denapaite D, Maurer P. Molecular mechanisms of β-lactam resistance in Streptococcus pneumoniae. Future Microbiol 2012; 7:395–410 [View Article] [PubMed]
    [Google Scholar]
  29. Chewapreecha C, Marttinen P, Croucher NJ, Salter SJ, Harris SR et al. Comprehensive identification of single nucleotide polymorphisms associated with beta-lactam resistance within pneumococcal mosaic genes. PLoS Genet 2014; 10:e1004547 [View Article] [PubMed]
    [Google Scholar]
  30. Chewapreecha C, Harris SR, Croucher NJ, Turner C, Marttinen P et al. Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet 2014; 46:305–309 [View Article] [PubMed]
    [Google Scholar]
  31. Coffey TJ, Dowson CG, Daniels M, Spratt BG. Horizontal spread of an altered penicillin-binding protein 2B gene between Streptococcus pneumoniae and Streptococcus oralis. FEMS Microbiol Lett 1993; 110:335–339 [View Article] [PubMed]
    [Google Scholar]
  32. Laible G, Spratt BG, Hakenbeck R. Interspecies recombinational events during the evolution of altered PBP 2x genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Mol Microbiol 1991; 5:1993–2002 [View Article] [PubMed]
    [Google Scholar]
  33. Muñoz R, Dowson CG, Daniels M, Coffey TJ, Martin C et al. Genetics of resistance to third-generation cephalosporins in clinical isolates of Streptococcus pneumoniae. Mol Microbiol 1992; 6:2461–2465 [View Article] [PubMed]
    [Google Scholar]
  34. Coffey TJ, Daniels M, McDougal LK, Dowson CG, Tenover FC et al. Genetic analysis of clinical isolates of Streptococcus pneumoniae with high-level resistance to expanded-spectrum cephalosporins. Antimicrob Agents Chemother 1995; 39:1306–1313 [View Article] [PubMed]
    [Google Scholar]
  35. Coffey TJ, Dowson CG, Daniels M, Zhou J, Martin C et al. Horizontal transfer of multiple penicillin-binding protein genes, and capsular biosynthetic genes, in natural populations of Streptococcus pneumoniae. Mol Microbiol 1991; 5:2255–2260 [View Article] [PubMed]
    [Google Scholar]
  36. Dowson CG, Hutchison A, Woodford N, Johnson AP, George RC et al. Penicillin-resistant viridans streptococci have obtained altered penicillin-binding protein genes from penicillin-resistant strains of Streptococcus pneumoniae. Proc Natl Acad Sci U S A 1990; 87:5858–5862 [View Article] [PubMed]
    [Google Scholar]
  37. Dowson CG, Hutchison A, Brannigan JA, George RC, Hansman D et al. Horizontal transfer of penicillin-binding protein genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Proc Natl Acad Sci U S A 1989; 86:8842–8846 [View Article] [PubMed]
    [Google Scholar]
  38. Dowson CG, Hutchison A, Spratt BG. Extensive re-modelling of the transpeptidase domain of penicillin-binding protein 2B of a penicillin-resistant South African isolate of Streptococcus pneumoniae. Mol Microbiol 1989; 3:95–102 [View Article] [PubMed]
    [Google Scholar]
  39. Dowson CG, Coffey TJ, Spratt BG. Origin and molecular epidemiology of penicillin-binding-protein-mediated resistance to β-lactam antibiotics. Trends Microbiol 1994; 2:361–366 [View Article] [PubMed]
    [Google Scholar]
  40. Enright MC, Spratt BG. Extensive variation in the ddl gene of penicillin-resistant Streptococcus pneumoniae results from a hitchhiking effect driven by the penicillin-binding protein 2b gene. Mol Biol Evol 1999; 16:1687–1695 [View Article] [PubMed]
    [Google Scholar]
  41. Feil EJ, Smith JM, Enright MC, Spratt BG. Estimating recombinational parameters in Streptococcus pneumoniae from multilocus sequence typing data. Genetics 2000; 154:1439–1450 [PubMed]
    [Google Scholar]
  42. Smith AM, Klugman KP, Coffey TJ, Spratt BG. Genetic diversity of penicillin-binding protein 2B and 2X genes from Streptococcus pneumoniae in South Africa. Antimicrob Agents Chemother 1993; 37:1938–1944 [View Article] [PubMed]
    [Google Scholar]
  43. Dowson CG, Coffey TJ, Kell C, Whiley RA. Evolution of penicillin resistance in Streptococcus pneumoniae; the role of Streptococcus mitis in the formation of a low affinity PBP2B in S. pneumoniae. Mol Microbiol 1993; 9:635–643 [View Article] [PubMed]
    [Google Scholar]
  44. Mostowy R, Croucher NJ, Andam CP, Corander J, Hanage WP et al. Efficient inference of recent and ancestral recombination within bacterial populations. Mol Biol Evol 2017; 34:1167–1182 [View Article] [PubMed]
    [Google Scholar]
  45. Marttinen P, Hanage WP, Croucher NJ, Connor TR, Harris SR et al. Detection of recombination events in bacterial genomes from large population samples. Nucleic Acids Res 2012; 40:e6 [View Article] [PubMed]
    [Google Scholar]
  46. Chi F, Nolte O, Bergmann C, Ip M, Hakenbeck R. Crossing the barrier: evolution and spread of a major class of mosaic pbp2x in Streptococcus pneumoniae, S. mitis and S. oralis. Int J Med Microbiol 2007; 297:503–512 [View Article]
    [Google Scholar]
  47. Sauerbier J, Maurer P, Rieger M, Hakenbeck R. Streptococcus pneumoniae R6 interspecies transformation: genetic analysis of penicillin resistance determinants and genome-wide recombination events. Mol Microbiol 2012; 86:692–706 [View Article] [PubMed]
    [Google Scholar]
  48. Jensen A, Valdórsson O, Frimodt-Møller N, Hollingshead S, Kilian M. Commensal streptococci serve as a reservoir for β-lactam resistance genes in Streptococcus pneumoniae. Antimicrob Agents Chemother 2015; 59:3529–3540 [View Article] [PubMed]
    [Google Scholar]
  49. Malhotra-Kumar S, Lammens C, Martel A, Mallentjer C, Chapelle S et al. Oropharyngeal carriage of macrolide-resistant viridans group streptococci: a prevalence study among healthy adults in Belgium. J Antimicrob Chemother 2004; 53:271–276 [View Article] [PubMed]
    [Google Scholar]
  50. Morita E, Narikiyo M, Nishimura E, Yano A, Tanabe C et al. Molecular analysis of age-related changes of Streptococcus anginosus group and Streptococcus mitis in saliva. Oral Microbiol Immunol 2004; 19:386–389 [View Article] [PubMed]
    [Google Scholar]
  51. Gladstone RA, SW L, Lees JA, Croucher NJ, van TA et al. International genomic definition of pneumococcal lineages, to contextualise disease, antibiotic resistance and vaccine impact. EBioMedicine 2019; 43:338–346 [View Article] [PubMed]
    [Google Scholar]
  52. Lo SW, Gladstone RA, van Tonder AJ, Lees JA, du Plessis M et al. Pneumococcal lineages associated with serotype replacement and antibiotic resistance in childhood invasive pneumococcal disease in the post-PCV13 era: an international whole-genome sequencing study. Lancet Infect Dis 2019; 19:759–769 [View Article] [PubMed]
    [Google Scholar]
  53. Wood DE, Salzberg SL. Kraken: ultrafast metagenomic sequence classification using exact alignments. Genome Biol 2014; 15:R46 [View Article] [PubMed]
    [Google Scholar]
  54. Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics 2013; 29:1072–1075 [View Article] [PubMed]
    [Google Scholar]
  55. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  56. Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015; 31:3691–3693 [View Article] [PubMed]
    [Google Scholar]
  57. Epping L, van Tonder AJ, Gladstone RA. The Global Pneumococcal Sequencing Consortium Bentley SD et al. SeroBA: rapid high-throughput serotyping of Streptococcus pneumoniae from whole genome sequence data. Microb Genom 2018; 4: [View Article]
    [Google Scholar]
  58. Jolley KA, Bray JE, Maiden MCJ. Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 2018; 3:124 [View Article] [PubMed]
    [Google Scholar]
  59. Lees JA, Harris SR, Tonkin-Hill G, Gladstone RA, Lo SW et al. Fast and flexible bacterial genomic epidemiology with PopPUNK. Genome Res 2019; 29:304–316 [View Article] [PubMed]
    [Google Scholar]
  60. Page AJ, Taylor B, Delaney AJ, Soares J, Seemann T et al. SNP-sites: rapid efficient extraction of SNPs from multi-FASTA alignments. Microb Genom 2016; 2:e000056 [View Article] [PubMed]
    [Google Scholar]
  61. Price MN, Dehal PS, Arkin AP. FastTree 2--approximately maximum-likelihood trees for large alignments. PLoS One 2010; 5:e9490 [View Article] [PubMed]
    [Google Scholar]
  62. Letunic I, Bork P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 2016; 44:245W242 [View Article] [PubMed]
    [Google Scholar]
  63. Argimón S, Abudahab K, Goater RJE, Fedosejev A, Bhai J et al. Microreact: visualizing and sharing data for genomic epidemiology and phylogeography. Microb Genom 2016; 2:e000093 [View Article] [PubMed]
    [Google Scholar]
  64. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997; 25:3389–3402 [View Article] [PubMed]
    [Google Scholar]
  65. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article] [PubMed]
    [Google Scholar]
  66. Cheng L, Connor TR, Sirén J, Aanensen DM, Corander J. Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Mol Biol Evol 2013; 30:1224–1228 [View Article] [PubMed]
    [Google Scholar]
  67. Mostowy RJ, Croucher NJ, De Maio N, Chewapreecha C, Salter SJ et al. Pneumococcal capsule synthesis locus cps as evolutionary hotspot with potential to generate novel serotypes by recombination. Mol Biol Evol 2017; 34:2537–2554 [View Article] [PubMed]
    [Google Scholar]
  68. Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P et al. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 2017; 34:3299–3302 [View Article] [PubMed]
    [Google Scholar]
  69. Wickham H. ggplot2: Elegant Graphics for Data Analysis Berlin: Springer; 2009
    [Google Scholar]
  70. R Core Team R: A Language and Environment for Statistical Computing Vienna, Austria: R Foundation for Statistical Computing; 2013
    [Google Scholar]
  71. Biçmen M, Gülay Z, Ramaswamy SV, Musher DM, Gür D. Analysis of mutations in the pbp genes of penicillin-non-susceptible pneumococci from Turkey. Clin Microbiol Infect 2006; 12:150–155 [View Article] [PubMed]
    [Google Scholar]
  72. Metcalf BJ, Chochua S, Gertz RE Jr, Li Z, Walker H et al. Using whole genome sequencing to identify resistance determinants and predict antimicrobial resistance phenotypes for year 2015 invasive pneumococcal disease isolates recovered in the United States. Clin Microbiol Infect 2016; 22:1002 [View Article]
    [Google Scholar]
  73. Li Y, Metcalf BJ, Chochua S, Li Z, Gertz RE et al. Validation of β-lactam minimum inhibitory concentration predictions for pneumococcal isolates with newly encountered penicillin binding protein (PBP) sequences. BMC Genomics 2017; 18:621 [View Article] [PubMed]
    [Google Scholar]
  74. Azarian T, Mitchell PK, Georgieva M, Thompson CM, Ghouila A et al. Global emergence and population dynamics of divergent serotype 3 CC180 pneumococci. PLoS Pathog 2018; 14:e1007438 [View Article] [PubMed]
    [Google Scholar]
  75. Beall B, Chochua S, Gertz RE, Li Y, Li Z et al. A population-based descriptive atlas of invasive pneumococcal strains recovered within the U.S. during 2015–2016. Front Microbiol 2018; 9:2670 [View Article] [PubMed]
    [Google Scholar]
  76. Chaguza C, Heinsbroek E, Gladstone RA, Tafatatha T, Alaerts M et al. Early signals of vaccine-driven perturbation seen in pneumococcal carriage population genomic data. Clin Infect Dis 2020; 70:1294–1303 [View Article] [PubMed]
    [Google Scholar]
  77. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003; 13:2498–2504 [View Article] [PubMed]
    [Google Scholar]
  78. Enright MC, Spratt BG. A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology (Reading) 1998; 144:3049–3060 [View Article] [PubMed]
    [Google Scholar]
  79. Hanage WP, Kaijalainen T, Herva E, Saukkoriipi A, Syrjänen R et al. Using multilocus sequence data to define the pneumococcus. J Bacteriol 2005; 187:6223–6230 [View Article] [PubMed]
    [Google Scholar]
  80. Kilian M, Poulsen K, Blomqvist T, Håvarstein LS, Bek-Thomsen M et al. Evolution of Streptococcus pneumoniae and its close commensal relatives. PLoS One 2008; 3:e2683 [View Article] [PubMed]
    [Google Scholar]
  81. Kilian M, Riley DR, Jensen A, Brüggemann H, Tettelin H. Parallel evolution of Streptococcus pneumoniae and Streptococcus mitis to pathogenic and mutualistic lifestyles. mBio 2014; 5:e01490-01414 [View Article] [PubMed]
    [Google Scholar]
  82. Diawara I, Nayme K, Katfy K, Barguigua A, Kettani-Halabi M et al. Analysis of amino acid motif of penicillin-binding proteins 1a, 2b, and 2x in invasive Streptococcus pneumoniae nonsusceptible to penicillin isolated from pediatric patients in Casablanca, Morocco. BMC Res Notes 2018; 11:632 [View Article] [PubMed]
    [Google Scholar]
  83. Nagai K, Davies TA, Jacobs MR, Appelbaum PC. Effects of amino acid alterations in penicillin-binding proteins (PBPs) 1a, 2b, and 2x on PBP affinities of penicillin, ampicillin, amoxicillin, cefditoren, cefuroxime, cefprozil, and cefaclor in 18 clinical isolates of penicillin-susceptible, -intermediate, and -resistant pneumococci. Antimicrob Agents Chemother 2002; 46:1273–1280 [View Article] [PubMed]
    [Google Scholar]
  84. Nichol KA, Zhanel GG, Hoban DJ. Penicillin-binding protein 1A, 2B, and 2X alterations in Canadian isolates of penicillin-resistant Streptococcus pneumoniae. Antimicrob Agents Chemother 2002; 46:3261–3264 [View Article] [PubMed]
    [Google Scholar]
  85. Biçmen M, Gülay Z, Ramaswamy SV, Musher DM, Gür D. Analysis of mutations in the pbp genes of penicillin-non-susceptible pneumococci from Turkey. Clin Microbiol Infect 2006; 12:150–155 [View Article] [PubMed]
    [Google Scholar]
  86. Gladstone RA, SW L, Lees JA, Croucher NJ, van Tonder AJ et al. International genomic definition of pneumococcal lineages, to contextualise disease, antibiotic resistance and vaccine impact. EBioMedicine 2019; 43:338–346 [View Article] [PubMed]
    [Google Scholar]
  87. Bast DJ, de AJ, Tam TY, Kilburn L, Duncan C et al. Interspecies recombination contributes minimally to fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob Agents Chemother 2001; 45:2631–2634 [View Article] [PubMed]
    [Google Scholar]
  88. Lehtinen S, Blanquart F, Croucher NJ, Turner P, Lipsitch M et al. Evolution of antibiotic resistance is linked to any genetic mechanism affecting bacterial duration of carriage. Proc Natl Acad Sci U S A 2017; 114:1075–1080 [View Article] [PubMed]
    [Google Scholar]
  89. Chaguza C, Andam CP, Harris SR, Cornick JE, Yang M et al. Recombination in Streptococcus pneumoniae lineages increase with carriage duration and size of the polysaccharide capsule. mBio 2016; 7:e01053-16 [View Article] [PubMed]
    [Google Scholar]
  90. Donati C, Hiller NL, Tettelin H, Muzzi A, Croucher NJ et al. Structure and dynamics of the pan-genome of Streptococcus pneumoniae and closely related species. Genome Biol 2010; 11:R107 [View Article] [PubMed]
    [Google Scholar]
  91. Didelot X, Maiden MCJ. Impact of recombination on bacterial evolution. Trends Microbiol 2010; 18:315 [View Article] [PubMed]
    [Google Scholar]
  92. Majewski J. Sexual isolation in bacteria. FEMS Microbiol Lett 2001; 199:161–169 [View Article] [PubMed]
    [Google Scholar]
  93. Lawrence JG. Gene transfer in bacteria: speciation without species. Theor Popul Biol 2002; 61:449–460 [View Article] [PubMed]
    [Google Scholar]
  94. van der Linden M, Otten J, Bergmann C, Latorre C, Liñares J et al. Insight into the diversity of penicillin-binding protein 2x alleles and mutations in viridans streptococci. Antimicrob Agents Chemother 2017; 61: [View Article] [PubMed]
    [Google Scholar]
  95. Adetifa IMO, Adamu AL, Karani A, Waithaka M, Odeyemi KA et al. Nasopharyngeal pneumococcal carriage in Nigeria: a two-site, population-based survey. Sci Rep 2018; 8:3509 [View Article] [PubMed]
    [Google Scholar]
  96. Turner P, Turner C, Jankhot A, Helen N, Lee SJ et al. A longitudinal study of Streptococcus pneumoniae carriage in a cohort of infants and their mothers on the Thailand–Myanmar border. PLoS One 2012; 7:e38271 [View Article] [PubMed]
    [Google Scholar]
  97. Hausdorff WP, Feikin DR, Klugman KP. Epidemiological differences among pneumococcal serotypes. Lancet Infect Dis 2005; 5:83–93 [View Article] [PubMed]
    [Google Scholar]
  98. Donkor ES, Bishop CJ, Gould K, Hinds J, Antonio M et al. High levels of recombination among Streptococcus pneumoniae isolates from the Gambia. mBio 2011; 2:e00040-11 [View Article] [PubMed]
    [Google Scholar]
  99. Hanage WP, Fraser C, Tang J, Connor TR, Hyper-Recombination CJ. Diversity, and antibiotic resistance in pneumococcus. Science 2009; 324:1454–1457 [View Article] [PubMed]
    [Google Scholar]
  100. Andam CP, Hanage WP. Mechanisms of genome evolution of Streptococcus. Infect Genet Evol 2015; 33:334–342 [View Article] [PubMed]
    [Google Scholar]
  101. Wyres KL, Lambertsen LM, Croucher NJ, McGee L, von Gottberg A et al. The multidrug-resistant PMEN1 pneumococcus is a paradigm for genetic success. Genome Biol 2012; 13:R103 [View Article] [PubMed]
    [Google Scholar]
  102. Mostowy R, Croucher NJ, Hanage WP, Harris SR, Bentley S et al. Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution. PLoS Genet 2014; 10:e1004300 [View Article] [PubMed]
    [Google Scholar]
  103. Pimenta F, Gertz RE, Park SH, Kim E, Moura I et al. Streptococcus infantis, Streptococcus mitis, and Streptococcus oralis strains with highly similar cps5 loci and antigenic relatedness to serotype 5 pneumococci. Front Microbiol 2018; 9:3199 [View Article] [PubMed]
    [Google Scholar]
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