1887

Microbial Genomics logo

Volume 9, Issue 7

Nasopharyngeal competition dynamics are likely to be altered following vaccine introduction: bacteriocin prevalence and diversity among Icelandic and Kenyan pneumococci Open Access

Abstract

Bacteriocins are antimicrobial peptides produced by bacteria to inhibit other bacteria in the surrounding environment. is a leading cause of disease worldwide and colonises the healthy human nasopharynx, where it competes for space and nutrients. Pneumococcal conjugate vaccines have reduced the incidence of disease, but they also restructure the bacterial population, and this restructuring likely alters the nasopharyngeal competition dynamics. Here, the distribution of bacteriocins was examined in over 5000 carriage and disease-causing pneumococci from Iceland and Kenya, recovered before and after the introduction of pneumococcal vaccination. Overall, up to eleven different bacteriocin gene clusters were identified per pneumococcus. Significant differences in the prevalence of bacteriocins were observed before and after vaccine introduction, and among carriage and disease-causing pneumococci, which were largely explained by the bacterial population structure. Genetically similar pneumococci generally harboured the same bacteriocins although sometimes different repertoires of bacteriocins were observed, which suggested that horizontal transfer of bacteriocin clusters had occurred. These findings demonstrated that vaccine-mediated changes in the pneumococcal population altered the prevalence and distribution of bacteriocins. The consequences of this for pneumococcal colonisation and disease remain to be determined.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacteriocins , competition , pneumococcus and vaccine-mediated changes
Funding
This study was supported by the:
  • Wellcome Trust (Award 218205/Z/19/Z)
    • Principle Award Recipient: AngelaB Brueggemann
  • Wellcome Trust (Award 098532)
    • Principle Award Recipient: JAnthony G Scott
  • Wellcome Trust (Award 215112/Z/18/Z)
    • Principle Award Recipient: MadeleineEB Butler
  • Wellcome Trust (Award 206394/Z/17/Z)
    • Principle Award Recipient: AngelaB Brueggemann
© 2023 The Authors
  • 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.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.001060
2023-07-12
2024-09-16
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/7/mgen001060.html?itemId=/content/journal/mgen/10.1099/mgen.0.001060&mimeType=html&fmt=ahah

References

  1. Butler ME, Rensburg MJJ van, Karani A, Mvera B, Akech D et al.Nasopharyngeal competition dynamics are likely to be altered following vaccine introduction: bacteriocin prevalence and diversity among Icelandic and Kenyan pneumococci Figshare 2023 https://doi.org/10.6084/m9.figshare.23266526.v1
     [Google Scholar]
  2. GBD 2016 Lower Respiratory Infections Collaborators Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory infections in 195 countries, 1990-2016: a systematic analysis for the global burden of disease study 2016. Lancet Infect Dis 2018; 18:1191–1210 [View Article] [PubMed]
     [Google Scholar]
  3. Tuomanen EI, Mitchell TJ, Morrison DA, Spratt BG. The Pneumococcus. ASM Press 2004 [View Article]
     [Google Scholar]
  4. Sleeman KL, Griffiths D, Shackley F, Diggle L, Gupta S et al. Capsular serotype-specific attack rates and duration of carriage of Streptococcus pneumoniae in a population of children. J Infect Dis 2006; 194:682–688 [View Article] [PubMed]
     [Google Scholar]
  5. Shak JR, Vidal JE, Klugman KP. Influence of bacterial interactions on pneumococcal colonization of the nasopharynx. Trends Microbiol 2013; 21:129–135 [View Article] [PubMed]
     [Google Scholar]
  6. Auranen K, Mehtälä J, Tanskanen A, S Kaltoft M. Between-strain competition in acquisition and clearance of pneumococcal carriage--epidemiologic evidence from a longitudinal study of day-care children. Am J Epidemiol 2010; 171:169–176 [View Article] [PubMed]
     [Google Scholar]
  7. Hammitt LL, Etyang AO, Morpeth SC, Ojal J, Mutuku A et al. Effect of ten-valent pneumococcal conjugate vaccine on invasive pneumococcal disease and nasopharyngeal carriage in Kenya: a longitudinal surveillance study. Lancet 2019; 393:2146–2154 [View Article] [PubMed]
     [Google Scholar]
  8. Quirk SJ, Haraldsson G, Erlendsdóttir H, Hjálmarsdóttir MÁ, van Tonder AJ et al. Effect of vaccination on pneumococci isolated from the nasopharynx of healthy children and the middle ear of children with otitis media in Iceland. J Clin Microbiol 2018; 56:e01046-18 [View Article] [PubMed]
     [Google Scholar]
  9. Quirk SJ, Haraldsson G, Hjálmarsdóttir MÁ, van Tonder AJ, Hrafnkelsson B et al. Vaccination of Icelandic children with the 10-valent pneumococcal vaccine leads to a significant herd effect among adults in Iceland. J Clin Microbiol 2019; 57:e01766-18 [View Article] [PubMed]
     [Google Scholar]
  10. Dawid S, Roche AM, Weiser JN. The blp bacteriocins of Streptococcus pneumoniae mediate intraspecies competition both in vitro and in vivo. Infect Immun 2007; 75:443–451 [View Article] [PubMed]
     [Google Scholar]
  11. Perez RH, Zendo T, Sonomoto K. Novel bacteriocins from lactic acid bacteria (LAB): various structures and applications. Microb Cell Fact 2014; 13 Suppl 1:S3 [View Article] [PubMed]
     [Google Scholar]
  12. Arnison PG, Bibb MJ, Bierbaum G, Bowers AA, Bugni TS et al. Ribosomally synthesized and post-translationally modified peptide natural products: overview and recommendations for a universal nomenclature. Nat Prod Rep 2013; 30:108–160 [View Article] [PubMed]
     [Google Scholar]
  13. Bogaardt C, van Tonder AJ, Brueggemann AB. Genomic analyses of pneumococci reveal a wide diversity of bacteriocins - including pneumocyclicin, a novel circular bacteriocin. BMC Genomics 2015; 16:554 [View Article] [PubMed]
     [Google Scholar]
  14. Wholey W-Y, Abu-Khdeir M, Yu EA, Siddiqui S, Esimai O et al. Characterization of the competitive pneumocin peptides of Streptococcus pneumoniae. Front Cell Infect Microbiol 2019; 9:55 [View Article] [PubMed]
     [Google Scholar]
  15. Rezaei Javan R, van Tonder AJ, King JP, Harrold CL, Brueggemann AB. Genome sequencing reveals a large and diverse repertoire of antimicrobial peptides. Front Microbiol 2018; 9:2012 [View Article] [PubMed]
     [Google Scholar]
  16. Begley M, Cotter PD, Hill C, Ross RP. Identification of a novel two-peptide lantibiotic, lichenicidin, following rational genome mining for LanM proteins. Appl Environ Microbiol 2009; 75:5451–5460 [View Article] [PubMed]
     [Google Scholar]
  17. Abdullahi O, Nyiro J, Lewa P, Slack M, Scott JAG. The descriptive epidemiology of Streptococcus pneumoniae and Haemophilus influenzae nasopharyngeal carriage in children and adults in Kilifi district, Kenya. Pediatr Infect Dis J 2008; 27:59–64 [View Article] [PubMed]
     [Google Scholar]
  18. Abdullahi O, Karani A, Tigoi CC, Mugo D, Kungu S et al. The prevalence and risk factors for pneumococcal colonization of the nasopharynx among children in Kilifi District, Kenya. PLoS One 2012; 7:e30787 [View Article] [PubMed]
     [Google Scholar]
  19. Abdullahi O, Karani A, Tigoi CC, Mugo D, Kungu S et al. Rates of acquisition and clearance of pneumococcal serotypes in the nasopharynges of children in Kilifi District, Kenya. J Infect Dis 2012; 206:1020–1029 [View Article] [PubMed]
     [Google Scholar]
  20. Hammitt LL, Akech DO, Morpeth SC, Karani A, Kihuha N et al. Population effect of 10-valent pneumococcal conjugate vaccine on nasopharyngeal carriage of Streptococcus pneumoniae and non-typeable Haemophilus influenzae in Kilifi, Kenya: findings from cross-sectional carriage studies. Lancet Glob Health 2014; 2:e397–405 [View Article] [PubMed]
     [Google Scholar]
  21. van Tonder AJ, Bray JE, Roalfe L, White R, Zancolli M et al. Genomics reveals the worldwide distribution of multidrug-resistant serotype 6E pneumococci. J Clin Microbiol 2015; 53:2271–2285 [View Article] [PubMed]
     [Google Scholar]
  22. van Tonder AJ, Bray JE, Quirk SJ, Haraldsson G, Jolley KA et al. Putatively novel serotypes and the potential for reduced vaccine effectiveness: capsular locus diversity revealed among 5405 pneumococcal genomes. Microb Genom 2016; 2:000090 [View Article] [PubMed]
     [Google Scholar]
  23. Zerbino DR. Using the Velvet de novo assembler for short-read sequencing technologies. Curr Protoc Bioinformatics 2010; Chapter 11:Unit [View Article] [PubMed]
     [Google Scholar]
  24. Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W. Scaffolding pre-assembled contigs using SSPACE. Bioinformatics 2011; 27:578–579 [View Article] [PubMed]
     [Google Scholar]
  25. Boetzer M, Pirovano W. Toward almost closed genomes with GapFiller. Genome Biol 2012; 13:R56 [View Article] [PubMed]
     [Google Scholar]
  26. Jolley KA, Maiden MCJ. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11:595 [View Article] [PubMed]
     [Google Scholar]
  27. Jolley KA, Bliss CM, Bennett JS, Bratcher HB, Brehony C et al. Ribosomal multilocus sequence typing: universal characterization of bacteria from domain to strain. Microbiology 2012; 158:1005–1015 [View Article] [PubMed]
     [Google Scholar]
  28. Francisco AP, Vaz C, Monteiro PT, Melo-Cristino J, Ramirez M et al. PHYLOViZ: phylogenetic inference and data visualization for sequence based typing methods. BMC Bioinformatics 2012; 13:87 [View Article] [PubMed]
     [Google Scholar]
  29. Epping L, van Tonder AJ, Gladstone RA, Bentley SD, Page AJ et al. SeroBA: rapid high-throughput serotyping of Streptococcus pneumoniae from whole genome sequence data.. Microb Genom 2018; 4:e000204 [View Article] [PubMed]
     [Google Scholar]
  30. Guiral S, Mitchell TJ, Martin B, Claverys J-P. Competence-programmed predation of noncompetent cells in the human pathogen Streptococcus pneumoniae: genetic requirements. Proc Natl Acad Sci 2005; 102:8710–8715 [View Article] [PubMed]
     [Google Scholar]
  31. Hoover SE, Perez AJ, Tsui H-C, Sinha D, Smiley DL et al. A new quorum-sensing system (TprA/PhrA) for Streptococcus pneumoniae D39 that regulates a lantibiotic biosynthesis gene cluster. Mol Microbiol 2015; 97:229–243 [View Article] [PubMed]
     [Google Scholar]
  32. Maricic N, Anderson ES, Opipari AE, Yu EA, Dawid S. Characterization of a multipeptide lantibiotic locus in Streptococcus pneumoniae. mBio 2016; 7:e01656 [View Article] [PubMed]
     [Google Scholar]
  33. Walker GV, Heng NCK, Carne A, Tagg JR, Wescombe PA. Salivaricin E and abundant dextranase activity may contribute to the anti-cariogenic potential of the probiotic candidate Streptococcus salivarius JH. Microbiology 2016; 162:476–486 [View Article] [PubMed]
     [Google Scholar]
  34. Croucher NJ, Walker D, Romero P, Lennard N, Paterson GK et al. Role of conjugative elements in the evolution of the multidrug-resistant pandemic clone Streptococcus pneumoniae Spain23F ST81. J Bacteriol 2009; 191:1480–1489 [View Article] [PubMed]
     [Google Scholar]
  35. Wyres KL, van Tonder A, Lambertsen LM, Hakenbeck R, Parkhill J et al. Evidence of antimicrobial resistance-conferring genetic elements among pneumococci isolated prior to 1974. BMC Genomics 2013; 14:500 [View Article] [PubMed]
     [Google Scholar]
  36. Ambroset C, Coluzzi C, Guédon G, Devignes M-D, Loux V et al. New insights into the classification and integration specificity of Streptococcus integrative conjugative elements through extensive genome exploration. Front Microbiol 2015; 6:1483 [View Article] [PubMed]
     [Google Scholar]
  37. Sun Y, Veseli IA, Vaillancourt K, Frenette M, Grenier D et al. The bacteriocin from the prophylactic candidate Streptococcus suis 90-1330 is widely distributed across S. suis isolates and appears encoded in an integrative and conjugative element. PLoS One 2019; 14:e0216002 [View Article] [PubMed]
     [Google Scholar]
  38. 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 1990; 87:5858–5862 [View Article] [PubMed]
     [Google Scholar]
  39. 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]
  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. Salvadori G, Junges R, Morrison DA, Petersen FC. Competence in Streptococcus pneumoniae and close commensal relatives: mechanisms and implications. Front Cell Infect Microbiol 2019; 9:94 [View Article] [PubMed]
     [Google Scholar]
/content/journal/mgen/10.1099/mgen.0.001060
Loading
Nasopharyngeal competition dynamics are likely to be altered following vaccine introduction: bacteriocin prevalence and diversity among Icelandic and Kenyan pneumococci
M Gen 9, 001060 (2023); https://doi.org/10.1099/mgen.0.001060
/content/journal/mgen/10.1099/mgen.0.001060
/content/journal/mgen/10.1099/mgen.0.001060
Loading

Data & Media loading...

Supplements

Loading data from figshare Loading data from figshare

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error