Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model

ABSTRACT Competitive interactions between Streptococcus pneumoniae strains during host colonization could influence the serotype distribution in nasopharyngeal carriage and pneumococcal disease. We evaluated the competitive fitness of strains of serotypes 6B, 14, 19A, 19F, 23F, and 35B in a mouse mo...

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Autores principales:	Krzysztof Trzciński, Yuan Li, Daniel M. Weinberger, Claudette M. Thompson, Derrick Cordy, Andrew Bessolo, Richard Malley, Marc Lipsitch
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e593570913224905921eb243ef95aeae
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spelling	oai:doaj.org-article:e593570913224905921eb243ef95aeae2021-11-15T15:41:30ZEffect of Serotype on Pneumococcal Competition in a Mouse Colonization Model10.1128/mBio.00902-152150-7511https://doaj.org/article/e593570913224905921eb243ef95aeae2015-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00902-15https://doaj.org/toc/2150-7511ABSTRACT Competitive interactions between Streptococcus pneumoniae strains during host colonization could influence the serotype distribution in nasopharyngeal carriage and pneumococcal disease. We evaluated the competitive fitness of strains of serotypes 6B, 14, 19A, 19F, 23F, and 35B in a mouse model of multiserotype carriage. Isogenic variants were constructed using clinical strains as the capsule gene donors. Animals were intranasally inoculated with a mixture of up to six pneumococcal strains of different serotypes, with separate experiments involving either clinical isolates or isogenic capsule-switch variants of clinical strain TIGR4. Upper-respiratory-tract samples were repeatedly collected from animals in order to monitor changes in the serotype ratios using quantitative PCR. A reproducible hierarchy of capsular types developed in the airways of mice inoculated with multiple strains. Serotype ranks in this hierarchy were similar among pneumococcal strains of different genetic backgrounds in different strains of mice and were not altered when tested under a range of host conditions. This rank correlated with the measure of the metabolic cost of capsule synthesis and in vitro measure of pneumococcal cell surface charge, both parameters considered to be predictors of serotype-specific fitness in carriage. This study demonstrates the presence of a robust competitive hierarchy of pneumococcal serotypes in vivo that is driven mainly, but not exclusively, by the capsule itself. IMPORTANCE Streptococcus pneumoniae (pneumococcus) is the leading cause of death due to respiratory bacterial infections but also a commensal frequently carried in upper airways. Available vaccines induce immune responses against polysaccharides coating pneumococcal cells, but with over 90 different capsular types (serotypes) identified, they can only target strains of the selected few serotypes most prevalent in disease. Vaccines not only protect vaccinated individuals against disease but also protect by reducing carriage of vaccine-targeted strains to induce herd effects across whole populations. Unfortunately, reduction in the circulation of vaccine-type strains is offset by increase in carriage and disease from nonvaccine strains, indicating the importance of competitive interactions between pneumococci in shaping the population structure of this pathogen. Here, we showed that the competitive ability of pneumococcal strains to colonize the host strongly depends on the type of capsular polysaccharide expressed by pneumococci and only to a lesser degree on strain or host genetic backgrounds or on variation in host immune responses.Krzysztof TrzcińskiYuan LiDaniel M. WeinbergerClaudette M. ThompsonDerrick CordyAndrew BessoloRichard MalleyMarc LipsitchAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 5 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Krzysztof Trzciński Yuan Li Daniel M. Weinberger Claudette M. Thompson Derrick Cordy Andrew Bessolo Richard Malley Marc Lipsitch Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model
description	ABSTRACT Competitive interactions between Streptococcus pneumoniae strains during host colonization could influence the serotype distribution in nasopharyngeal carriage and pneumococcal disease. We evaluated the competitive fitness of strains of serotypes 6B, 14, 19A, 19F, 23F, and 35B in a mouse model of multiserotype carriage. Isogenic variants were constructed using clinical strains as the capsule gene donors. Animals were intranasally inoculated with a mixture of up to six pneumococcal strains of different serotypes, with separate experiments involving either clinical isolates or isogenic capsule-switch variants of clinical strain TIGR4. Upper-respiratory-tract samples were repeatedly collected from animals in order to monitor changes in the serotype ratios using quantitative PCR. A reproducible hierarchy of capsular types developed in the airways of mice inoculated with multiple strains. Serotype ranks in this hierarchy were similar among pneumococcal strains of different genetic backgrounds in different strains of mice and were not altered when tested under a range of host conditions. This rank correlated with the measure of the metabolic cost of capsule synthesis and in vitro measure of pneumococcal cell surface charge, both parameters considered to be predictors of serotype-specific fitness in carriage. This study demonstrates the presence of a robust competitive hierarchy of pneumococcal serotypes in vivo that is driven mainly, but not exclusively, by the capsule itself. IMPORTANCE Streptococcus pneumoniae (pneumococcus) is the leading cause of death due to respiratory bacterial infections but also a commensal frequently carried in upper airways. Available vaccines induce immune responses against polysaccharides coating pneumococcal cells, but with over 90 different capsular types (serotypes) identified, they can only target strains of the selected few serotypes most prevalent in disease. Vaccines not only protect vaccinated individuals against disease but also protect by reducing carriage of vaccine-targeted strains to induce herd effects across whole populations. Unfortunately, reduction in the circulation of vaccine-type strains is offset by increase in carriage and disease from nonvaccine strains, indicating the importance of competitive interactions between pneumococci in shaping the population structure of this pathogen. Here, we showed that the competitive ability of pneumococcal strains to colonize the host strongly depends on the type of capsular polysaccharide expressed by pneumococci and only to a lesser degree on strain or host genetic backgrounds or on variation in host immune responses.
format	article
author	Krzysztof Trzciński Yuan Li Daniel M. Weinberger Claudette M. Thompson Derrick Cordy Andrew Bessolo Richard Malley Marc Lipsitch
author_facet	Krzysztof Trzciński Yuan Li Daniel M. Weinberger Claudette M. Thompson Derrick Cordy Andrew Bessolo Richard Malley Marc Lipsitch
author_sort	Krzysztof Trzciński
title	Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model
title_short	Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model
title_full	Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model
title_fullStr	Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model
title_full_unstemmed	Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model
title_sort	effect of serotype on pneumococcal competition in a mouse colonization model
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/e593570913224905921eb243ef95aeae
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Effect of Serotype on Pneumococcal Competition in a Mouse Colonization Model

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