1887

Abstract

Serotype 1 is a leading cause of invasive pneumococcal disease (IPD) worldwide, with the highest burden in developing countries. We report the whole-genome sequencing analysis of 448 serotype 1 isolates from 27 countries worldwide (including 11 in Africa). The global serotype 1 population shows a strong phylogeographic structure at the continental level, and within Africa there is further region-specific structure. Our results demonstrate that region-specific diversification within Africa has been driven by limited cross-region transfer events, genetic recombination and antimicrobial selective pressure. Clonal replacement of the dominant serotype 1 clones circulating within regions is uncommon; however, here we report on the accessory gene content that has contributed to a rare clonal replacement event of ST3081 with ST618 as the dominant cause of IPD in the Gambia.

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2015-08-11
2019-09-15
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References

  1. Antonio M. , Hakeem I. , Awine T. , Secka O. , Sankareh K. , Nsekpong D. , Lahai G. , Akisanya A. , Egere U. , other authors . ( 2008;). Seasonality and outbreak of a predominant Streptococcus pneumoniae serotype 1 clone from The Gambia: expansion of ST217 hypervirulent clonal complex in West Africa. BMC Microbiol 8: 198 [CrossRef].[PubMed].
    [Google Scholar]
  2. Bentley S.D. , Aanensen D.M. , Mavroidi A. , Saunders D. , Rabbinowitsch E. , Collins M. , Donohoe K. , Harris D. , Murphy L. , other authors . ( 2006;). Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet 2: e31 [CrossRef] [PubMed].
    [Google Scholar]
  3. Blumental S. , Moïsi J.C. , Roalfe L. , Zancolli M. , Johnson M. , Burbidge P. , Borrow R. , Yaro S. , Mueller J.E. , other authors . ( 2015;). Streptococcus pneumoniae serotype 1 burden in the African meningitis belt: exploration of functionality in specific antibodies. Clin Vaccine Immunol 22: 404–412 [CrossRef].
    [Google Scholar]
  4. Boetzer M. , Henkel C.V. , Jansen H.J. , Butler D. , Pirovano W. . ( 2011;). Scaffolding pre-assembled contigs using sspace. Bioinformatics 27: 578–579 [CrossRef] [PubMed].
    [Google Scholar]
  5. Brueggemann A.B. , Spratt B.G. . ( 2003;). Geographic distribution and clonal diversity of Streptococcus pneumoniae serotype 1 isolates. J Clin Microbiol 41: 4966–4970 [CrossRef].[PubMed].
    [Google Scholar]
  6. Brueggemann A.B. , Griffiths D.T. , Meats E. , Peto T. , Crook D.W. , Spratt B.G. . ( 2003;). Clonal relationships between invasive and carriage Streptococcus pneumoniae and serotype- and clone-specific differences in invasive disease potential. J Infect Dis 187: 1424–1432 [CrossRef] [PubMed].
    [Google Scholar]
  7. Chalker A.F. , Lupas A. , Ingraham K. , So C.Y. , Lunsford R.D. , Li T. , Bryant A. , Holmes D.J. , Marra A. , other authors . ( 2000;). Genetic characterization of gram-positive homologs of the XerCD site-specific recombinases. J Mol Microbiol Biotechnol 2: 225–233 [PubMed]
    [Google Scholar]
  8. Chan P.F. , O'Dwyer K.M. , Palmer L.M. , Ambrad J.D. , Ingraham K.A. , So C. , Lonetto M.A. , Biswas S. , Rosenberg M. , other authors . ( 2003;). Characterization of a novel fucose-regulated promoter (PfcsK) suitable for gene essentiality and antibacterial mode-of-action studies in Streptococcus pneumoniae . J Bacteriol 185: 2051–2058 [CrossRef] [PubMed].
    [Google Scholar]
  9. Chewapreecha C. , Harris S.R. , Croucher N.J. , Turner C. , Marttinen P. , Cheng L. , Pessia A. , Aanensen D.M. , Mather A.E. , other authors . ( 2014;). Dense genomic sampling identifies highways of pneumococcal recombination. Nat Genet 46: 305–309 [CrossRef] [PubMed].
    [Google Scholar]
  10. Cornick J.E. , Bentley S.D. . ( 2012;). Streptococcus pneumoniae: the evolution of antimicrobial resistance to beta-lactams, fluoroquinolones and macrolides. Microbes Infect 14: 573–583 [CrossRef] [PubMed].
    [Google Scholar]
  11. Cornick J.E. , Harris S.R. , Parry C.M. , Moore M.J. , Jassi C. , Kamng'ona A. , Kulohoma B. , Heyderman R.S. , Bentley S.D. , Everett D.B. . ( 2014;). Genomic identification of a novel co-trimoxazole resistance genotype and its prevalence amongst Streptococcus pneumoniae in Malawi. J Antimicrob Chemother 69: 368–374 [PubMed].[CrossRef]
    [Google Scholar]
  12. Croucher N.J. , Harris S.R. , Fraser C. , Quail M.A. , Burton J. , van der Linden M. , McGee L. , von Gottberg A. , Song J.H. , other authors . ( 2011;). Rapid pneumococcal evolution in response to clinical interventions. Science 331: 430–434 [CrossRef] [PubMed].
    [Google Scholar]
  13. Croucher N.J. , Finkelstein J.A. , Pelton S.I. , Mitchell P.K. , Lee G.M. , Parkhill J. , Bentley S.D. , Hanage W.P. , Lipsitch M. . ( 2013;). Population genomics of post-vaccine changes in pneumococcal epidemiology. Nat Genet 45: 656–663 [CrossRef] [PubMed].
    [Google Scholar]
  14. Croucher N.J. , Page A.J. , Connor T.R. , Delaney A.J. , Keane J.A. , Bentley S.D. , Parkhill J. , Harris S.R. . ( 2015;). Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res Nucleic Acids Res 43: e15 [PubMed].[CrossRef]
    [Google Scholar]
  15. Cutts F.T. , Zaman S.M.A. , Enwere G. , Jaffar S. , Levine O.S. , Okoko J.B. , Oluwalana C. , Vaughan A. , Obaro S.K. , other authors . ( 2005;). Efficacy of nine-valent pneumococcal conjugate vaccine against pneumonia and invasive pneumococcal disease in The Gambia: randomised, double-blind, placebo-controlled trial. Lancet 365: 1139–1146 [CrossRef] [PubMed].
    [Google Scholar]
  16. Dagan R. , Gradstein S. , Belmaker I. , Porat N. , Siton Y. , Weber G. , Janco J. , Yagupsky P. . ( 2000;). An outbreak of Streptococcus pneumoniae serotype 1 in a closed community in southern Israel. Clin Infect Dis 30: 319–321 [CrossRef] [PubMed].
    [Google Scholar]
  17. Delcher A.L. , Harmon D. , Kasif S. , White O. , Salzberg S.L. . ( 1999;). Improved microbial gene identification with glimmer. Nucleic Acids Res 27: 4636–4641 [CrossRef] [PubMed].
    [Google Scholar]
  18. Drummond A.J. , Suchard M.A. , Xie D. , Rambaut A. . ( 2012;). Bayesian phylogenetics with BEAUti and the beast 1.7. Mol Biol Evol 29: 1969–1973 [CrossRef] [PubMed].
    [Google Scholar]
  19. Embry A. , Hinojosa E. , Orihuela C.J. . ( 2007;). Regions of Diversity 8, 9 and 13 contribute to Streptococcus pneumoniae virulence. BMC Microbiol 7: 80 [CrossRef] [PubMed].
    [Google Scholar]
  20. Everett D.B. , Mukaka M. , Denis B. , Gordon S.B. , Carrol E.D. , van Oosterhout J.J. , Molyneux E.M. , Molyneux M. , French N. , Heyderman R.S. . ( 2011;). Ten years of surveillance for invasive Streptococcus pneumoniae during the era of antiretroviral scale-up and cotrimoxazole prophylaxis in Malawi. PLoS One 6: e17765 [CrossRef] [PubMed].
    [Google Scholar]
  21. Harboe Z.B. , Benfield T.L. , Valentiner-Branth P. , Hjuler T. , Lambertsen L. , Kaltoft M. , Krogfelt K. , Slotved H.C. , Christensen J.J. , Konradsen H.B. . ( 2010;). Temporal trends in invasive pneumococcal disease and pneumococcal serotypes over 7 decades. Clin Infect Dis 50: 329–337 [CrossRef] [PubMed].
    [Google Scholar]
  22. Harris S.R. , Feil E.J. , Holden M.T. , Quail M.A. , Nickerson E.K. , Chantratita N. , Gardete S. , Tavares A. , Day N. , other authors . ( 2010;). Evolution of MRSA during hospital transmission and intercontinental spread. Science 327: 469–474 [CrossRef] [PubMed].
    [Google Scholar]
  23. Hausdorff W.P. , Feikin D.R. , Klugman K.P. . ( 2005;). Epidemiological differences among pneumococcal serotypes. Lancet Infect Dis 5: 83–93 [CrossRef] [PubMed].
    [Google Scholar]
  24. Higgins M.A. , Abbott D.W. , Boulanger M.J. , Boraston A.B. . ( 2009;). Blood group antigen recognition by a solute-binding protein from a serotype 3 strain of Streptococcus pneumoniae . J Mol Biol 388: 299–309 [CrossRef] [PubMed].
    [Google Scholar]
  25. Inouye M. , Conway T.C. , Zobel J. , Holt K.E. . ( 2012;). Short read sequence typing (SRST): multi-locus sequence types from short reads. BMC Genomics 13: 338 [CrossRef] [PubMed].
    [Google Scholar]
  26. Iyer J.K. , Milhous W.K. , Cortese J.F. , Kublin J.G. , Plowe C.V. . ( 2001;). Plasmodium falciparum cross-resistance between trimethoprim and pyrimethamine. Lancet 358: 1066–1067 [CrossRef] [PubMed].
    [Google Scholar]
  27. Johnson H.L. , Deloria-Knoll M. , Levine O.S. , Stoszek S.K. , Freimanis Hance L. , Reithinger R. , Muenz L.R. , O'Brien K.L. . ( 2010;). Systematic evaluation of serotypes causing invasive pneumococcal disease among children under five: the pneumococcal global serotype project. PLoS Med 7: e1000348 [CrossRef] [PubMed].
    [Google Scholar]
  28. Klugman K.P. , Madhi S.A. , Huebner R.E. , Kohberger R. , Mbelle N. , Pierce N. , Vaccine Trialists Group . ( 2003;). A trial of a 9-valent pneumococcal conjugate vaccine in children with and those without HIV infection. N Engl J Med 349: 1341–1348 [CrossRef] [PubMed].
    [Google Scholar]
  29. Klugman K. , Cutts F. , Adegbola R.A. , Black S. , Madhi S.A. , O'Brien K. , Santosham M. , Shinefield H. . ( 2008;). Meta-analysis of the efficacy of conjugate vaccines against invasive pneumococcal disease. . In Pneumococcal Vaccines, pp. 317–326. Edited by Siber G. , Klugman K. , Mäkelä P. . Washington, DC: American Society for Microbiology; [CrossRef].
    [Google Scholar]
  30. Köser C.U. , Holden M.T. , Ellington M.J. , Cartwright E.J. , Brown N.M. , Ogilvy-Stuart A.L. , Hsu L.Y. , Chewapreecha C. , Croucher N.J. , other authors . ( 2012;). Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med 366: 2267–2275 [CrossRef] [PubMed].
    [Google Scholar]
  31. Le Bourgeois P. , Bugarel M. , Campo N. , Daveran-Mingot M.L. , Labonté J. , Lanfranchi D. , Lautier T. , Pagès C. , Ritzenthaler P. . ( 2007;). The unconventional Xer recombination machinery of streptococci/lactococci. PLoS Genet 3: e117 [PubMed].[CrossRef]
    [Google Scholar]
  32. Letunic I. , Bork P. . ( 2011;). Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39: W475–W478 [CrossRef] [PubMed].
    [Google Scholar]
  33. Li H. , Durbin R. . ( 2009;). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760 [CrossRef] [PubMed].
    [Google Scholar]
  34. Li L. , Stoeckert C.J. Jr , Roos D.S. . ( 2003;). OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189 [CrossRef] [PubMed].
    [Google Scholar]
  35. Li M.-F. , Zhang B.-C. , Li J. , Sun L. . ( 2014;). Sil: a Streptococcus iniae bacteriocin with dual role as an antimicrobial and an immunomodulator that inhibits innate immune response and promotes S. iniae infection. PLoS One 9: e96222 [CrossRef] [PubMed].
    [Google Scholar]
  36. Mukouhara T. , Arimoto T. , Cho K. , Yamamoto M. , Igarashi T. . ( 2011;). Surface lipoprotein PpiA of Streptococcus mutans suppresses scavenger receptor MARCO-dependent phagocytosis by macrophages. Infect Immun 79: 4933–4940 [CrossRef] [PubMed].
    [Google Scholar]
  37. O'Brien K.L. , Wolfson L.J. , Watt J.P. , Henkle E. , Deloria-Knoll M. , McCall N. , Lee E. , Mulholland K. , Levine O.S. , Cherian T. , Hib and Pneumococcal Global Burden of Disease Study Team . ( 2009;). Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374: 893–902 [CrossRef] [PubMed].
    [Google Scholar]
  38. Pai R. , Moore M.R. , Pilishvili T. , Gertz R.E. , Whitney C.G. , Beall B. , Active Bacterial Core Surveillance Team . ( 2005;). Postvaccine genetic structure of Streptococcus pneumoniae serotype 19A from children in the United States. J Infect Dis 192: 1988–1995 [CrossRef] [PubMed].
    [Google Scholar]
  39. United Nations High Commissioner for Refugees ( 2000;). The State of the World's Refugees, 2000: Fifty Years of Humanitarian Action Oxford: Oxford University Press;.
    [Google Scholar]
  40. Ritchie N.D. , Mitchell T.J. , Evans T.J. . ( 2012;). What is different about serotype 1 pneumococci?. Future Microbiol 7: 33–46 [CrossRef] [PubMed].
    [Google Scholar]
  41. Seemann T. . ( 2014;). Prokka: rapid prokaryotic genome annotation. Bioinformatics 30: 2068–2069 [CrossRef] [PubMed].
    [Google Scholar]
  42. Stamatakis A. . ( 2006;). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688–2690 [CrossRef] [PubMed].
    [Google Scholar]
  43. Turner P. , Turner C. , Jankhot A. , Helen N. , Lee S.J. , Day N.P. , White N.J. , Nosten F. , Goldblatt D. . ( 2012;). A longitudinal study of Streptococcus pneumoniae carriage in a cohort of infants and their mothers on the Thailand-Myanmar border. PLoS One 7: e38271 [CrossRef] [PubMed].
    [Google Scholar]
  44. Williams T.M. , Loman N.J. , Ebruke C. , Musher D.M. , Adegbola R.A. , Pallen M.J. , Weinstock G.M. , Antonio M. . ( 2012;). Genome analysis of a highly virulent serotype 1 strain of Streptococcus pneumoniae from West Africa. PLoS One 7: e26742 [CrossRef] [PubMed].
    [Google Scholar]
  45. Yildirim I. , Hanage W.P. , Lipsitch M. , Shea K.M. , Stevenson A. , Finkelstein J. , Huang S.S. , Lee G.M. , Kleinman K. , Pelton S.I. . ( 2010;). Serotype specific invasive capacity and persistent reduction in invasive pneumococcal disease. Vaccine 29: 283–288 [CrossRef] [PubMed].
    [Google Scholar]
  46. Zerbino D.R. , Birney E. . ( 2008;). Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 18: 821–829 [CrossRef] [PubMed].
    [Google Scholar]
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