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

Madeleine E. B Butler; Melissa J. Jansen van  Rensburg; Angela  Karani; Benedict  Mvera; Asma Akter; Donald  Akech; Calum h Forrest; Andries J. van  Tonder; Sigríður J.   Quirk; Gunnsteinn  Haraldsson; Stephen D.  Bentley; Helga  Erlendsdóttir; Ásgeir  Haraldsson; Karl G.  Kristinsson; J. Anthony G.  Scott; Angela B.  Brueggemann

doi:10.1099/mgen.0.001060

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

Madeleine E. B Butler, Melissa J. Jansen van Rensburg, Angela Karani, Benedict Mvera, Asma Akter, Donald Akech, Calum h Forrest, Andries J. van Tonder, Sigríður J. Quirk, Gunnsteinn Haraldsson, Stephen D. Bentley, Helga Erlendsdóttir, Ásgeir Haraldsson, Karl G. Kristinsson, J. Anthony G. Scott, Angela B. Brueggemann^*

^*Corresponding author for this work

Analytical, Environmental & Forensic Sciences

Research output: Contribution to journal › Article › peer-review

Abstract

Bacteriocins are antimicrobial peptides produced by bacteria to inhibit other bacteria in the surrounding environment. Streptococcus pneumoniae 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.

Original language	English
Article number	001060
Journal	Microbial Genomics
Volume	9
Issue number	7
DOIs	https://doi.org/10.1099/mgen.0.001060
Publication status	Published - 12 Jul 2023

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Butler, M. E. B., Rensburg, M. J. J. V., Karani, A., Mvera, B., Akter, A., Akech, D., Forrest, C. H., Tonder, A. J. V., Quirk, S. J., Haraldsson, G., Bentley, S. D., Erlendsdóttir, H., Haraldsson, Á., Kristinsson, K. G., Scott, J. A. G., & Brueggemann, A. B. (2023). Nasopharyngeal competition dynamics are likely to be altered following vaccine introduction: bacteriocin prevalence and diversity among Icelandic and Kenyan pneumococci. Microbial Genomics, 9(7), Article 001060. https://doi.org/10.1099/mgen.0.001060

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title = "Nasopharyngeal competition dynamics are likely to be altered following vaccine introduction: bacteriocin prevalence and diversity among Icelandic and Kenyan pneumococci",

abstract = "Bacteriocins are antimicrobial peptides produced by bacteria to inhibit other bacteria in the surrounding environment. Streptococcus pneumoniae 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.",

author = "Butler, {Madeleine E. B} and Rensburg, {Melissa J. Jansen van} and Angela Karani and Benedict Mvera and Asma Akter and Donald Akech and Forrest, {Calum h} and Tonder, {Andries J. van} and Quirk, {Sigr{\'i}{\dh}ur J.} and Gunnsteinn Haraldsson and Bentley, {Stephen D.} and Helga Erlendsd{\'o}ttir and {\'A}sgeir Haraldsson and Kristinsson, {Karl G.} and Scott, {J. Anthony G.} and Brueggemann, {Angela B.}",

note = "Funding Information: This work was funded by a Wellcome Trust Investigator Award to ABB (206394/Z/17/Z). MEBB was funded by a Wellcome Trust PhD Studentship (215112/Z/18/Z). JAGS was funded by a Wellcome Trust Senior Research Fellowship (098532). The PubMLST infrastructure is funded by a Wellcome Trust Biomedical Resource Grant awarded to ABB, Professor Martin CJ Maiden and Dr Keith A Jolley at the University of Oxford (218205/Z/19/Z). Publisher Copyright: {\textcopyright} 2023 The Authors.",

year = "2023",

month = jul,

day = "12",

doi = "10.1099/mgen.0.001060",

language = "English",

volume = "9",

journal = "Microbial Genomics",

issn = "2057-5858",

publisher = "Microbiology Society",

number = "7",

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Butler, MEB, Rensburg, MJJV, Karani, A, Mvera, B, Akter, A, Akech, D, Forrest, CH, Tonder, AJV, Quirk, SJ, Haraldsson, G, Bentley, SD, Erlendsdóttir, H, Haraldsson, Á, Kristinsson, KG, Scott, JAG & Brueggemann, AB 2023, 'Nasopharyngeal competition dynamics are likely to be altered following vaccine introduction: bacteriocin prevalence and diversity among Icelandic and Kenyan pneumococci', Microbial Genomics, vol. 9, no. 7, 001060. https://doi.org/10.1099/mgen.0.001060

Nasopharyngeal competition dynamics are likely to be altered following vaccine introduction: bacteriocin prevalence and diversity among Icelandic and Kenyan pneumococci. / Butler, Madeleine E. B; Rensburg, Melissa J. Jansen van; Karani, Angela et al.
In: Microbial Genomics, Vol. 9, No. 7, 001060, 12.07.2023.

Research output: Contribution to journal › Article › peer-review

TY - JOUR

T1 - Nasopharyngeal competition dynamics are likely to be altered following vaccine introduction

T2 - bacteriocin prevalence and diversity among Icelandic and Kenyan pneumococci

AU - Butler, Madeleine E. B

AU - Rensburg, Melissa J. Jansen van

AU - Karani, Angela

AU - Mvera, Benedict

AU - Akter, Asma

AU - Akech, Donald

AU - Forrest, Calum h

AU - Tonder, Andries J. van

AU - Quirk, Sigríður J.

AU - Haraldsson, Gunnsteinn

AU - Bentley, Stephen D.

AU - Erlendsdóttir, Helga

AU - Haraldsson, Ásgeir

AU - Kristinsson, Karl G.

AU - Scott, J. Anthony G.

AU - Brueggemann, Angela B.

N1 - Funding Information: This work was funded by a Wellcome Trust Investigator Award to ABB (206394/Z/17/Z). MEBB was funded by a Wellcome Trust PhD Studentship (215112/Z/18/Z). JAGS was funded by a Wellcome Trust Senior Research Fellowship (098532). The PubMLST infrastructure is funded by a Wellcome Trust Biomedical Resource Grant awarded to ABB, Professor Martin CJ Maiden and Dr Keith A Jolley at the University of Oxford (218205/Z/19/Z). Publisher Copyright: © 2023 The Authors.

PY - 2023/7/12

Y1 - 2023/7/12

N2 - Bacteriocins are antimicrobial peptides produced by bacteria to inhibit other bacteria in the surrounding environment. Streptococcus pneumoniae 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.

AB - Bacteriocins are antimicrobial peptides produced by bacteria to inhibit other bacteria in the surrounding environment. Streptococcus pneumoniae 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.

UR - http://www.scopus.com/inward/record.url?scp=85164624531&partnerID=8YFLogxK

U2 - 10.1099/mgen.0.001060

DO - 10.1099/mgen.0.001060

M3 - Article

SN - 2057-5858

VL - 9

JO - Microbial Genomics

JF - Microbial Genomics

IS - 7

M1 - 001060

ER -

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

Abstract

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