Capsule Type and Amount Affect Shedding and Transmission of <italic toggle="yes">Streptococcus pneumoniae</italic>

ABSTRACT The capsular polysaccharide (CPS) of Streptococcus pneumoniae is characterized by its diversity, as it has over 95 known serotypes, and the variation in its thickness as it surrounds an organism. While within-host effects of CPS have been studied in detail, there is no information about its...

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Autores principales: M. Ammar Zafar, Shigeto Hamaguchi, Tonia Zangari, Michael Cammer, Jeffrey N. Weiser
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:ef71bfb9e4554d8f846479285a18232d2021-11-15T15:51:43ZCapsule Type and Amount Affect Shedding and Transmission of <italic toggle="yes">Streptococcus pneumoniae</italic>10.1128/mBio.00989-172150-7511https://doaj.org/article/ef71bfb9e4554d8f846479285a18232d2017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00989-17https://doaj.org/toc/2150-7511ABSTRACT The capsular polysaccharide (CPS) of Streptococcus pneumoniae is characterized by its diversity, as it has over 95 known serotypes, and the variation in its thickness as it surrounds an organism. While within-host effects of CPS have been studied in detail, there is no information about its contribution to host-to-host transmission. In this study, we used an infant mouse model of intralitter transmission, together with isogenic capsule switch and cps promoter switch constructs, to explore the effects of CPS type and amount. The determining factor in the transmission rate in this model is the number of pneumococci shed in nasal secretions by colonized hosts. Two of seven capsule switch constructs showed reduced shedding. These constructs were unimpaired in colonization and expressed capsules similar in size to those of the wild-type strain. A cps promoter switch mutant expressing ~50% of wild-type amounts of CPS also displayed reduced shedding without a defect in colonization. Since shedding from the mucosal surface may require escape from mucus entrapment, a mucin-binding assay was used to compare capsule switch and cps promoter switch mutants. The CPS type or amount constructs that shed poorly were bound more robustly by immobilized mucin. These capsule switch and cps promoter switch constructs with increased mucin-binding affinity and reduced shedding also had lower rates of pup-to-pup transmission. Our results demonstrate that CPS type and amount affect transmission dynamics and may contribute to the marked differences in prevalence among pneumococcal types. IMPORTANCE Streptococcus pneumoniae, a leading cause of morbidity and mortality, is readily transmitted, especially among young children. Its structurally and antigenically diverse capsular polysaccharide is the target of currently licensed pneumococcal vaccines. Epidemiology studies show that only a subset of the >95 distinct serotypes are prevalent in the human population, suggesting that certain capsular polysaccharide types might be more likely to be transmitted within the community. Herein, we used an infant mouse model to show that both capsule type and amount are important determinants in the spread of pneumococci from host to host. Transmission rates correlate with those capsule types that are better at escaping mucus entrapment, a key step in exiting the host upper respiratory tract. Hence, our study provides a better mechanistic understanding of why certain pneumococcal serotypes are more common in the human population.M. Ammar ZafarShigeto HamaguchiTonia ZangariMichael CammerJeffrey N. WeiserAmerican Society for MicrobiologyarticleStreptococcus pneumoniaetransmissionbacterial sheddingcapsular polysaccharidehost-pathogen interactionsinfluenza AMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution DOAJ
collection DOAJ
language EN
topic Streptococcus pneumoniae
transmission
bacterial shedding
capsular polysaccharide
host-pathogen interactions
influenza A
Microbiology
QR1-502
spellingShingle Streptococcus pneumoniae
transmission
bacterial shedding
capsular polysaccharide
host-pathogen interactions
influenza A
Microbiology
QR1-502
M. Ammar Zafar
Shigeto Hamaguchi
Tonia Zangari
Michael Cammer
Jeffrey N. Weiser
Capsule Type and Amount Affect Shedding and Transmission of <italic toggle="yes">Streptococcus pneumoniae</italic>
description ABSTRACT The capsular polysaccharide (CPS) of Streptococcus pneumoniae is characterized by its diversity, as it has over 95 known serotypes, and the variation in its thickness as it surrounds an organism. While within-host effects of CPS have been studied in detail, there is no information about its contribution to host-to-host transmission. In this study, we used an infant mouse model of intralitter transmission, together with isogenic capsule switch and cps promoter switch constructs, to explore the effects of CPS type and amount. The determining factor in the transmission rate in this model is the number of pneumococci shed in nasal secretions by colonized hosts. Two of seven capsule switch constructs showed reduced shedding. These constructs were unimpaired in colonization and expressed capsules similar in size to those of the wild-type strain. A cps promoter switch mutant expressing ~50% of wild-type amounts of CPS also displayed reduced shedding without a defect in colonization. Since shedding from the mucosal surface may require escape from mucus entrapment, a mucin-binding assay was used to compare capsule switch and cps promoter switch mutants. The CPS type or amount constructs that shed poorly were bound more robustly by immobilized mucin. These capsule switch and cps promoter switch constructs with increased mucin-binding affinity and reduced shedding also had lower rates of pup-to-pup transmission. Our results demonstrate that CPS type and amount affect transmission dynamics and may contribute to the marked differences in prevalence among pneumococcal types. IMPORTANCE Streptococcus pneumoniae, a leading cause of morbidity and mortality, is readily transmitted, especially among young children. Its structurally and antigenically diverse capsular polysaccharide is the target of currently licensed pneumococcal vaccines. Epidemiology studies show that only a subset of the >95 distinct serotypes are prevalent in the human population, suggesting that certain capsular polysaccharide types might be more likely to be transmitted within the community. Herein, we used an infant mouse model to show that both capsule type and amount are important determinants in the spread of pneumococci from host to host. Transmission rates correlate with those capsule types that are better at escaping mucus entrapment, a key step in exiting the host upper respiratory tract. Hence, our study provides a better mechanistic understanding of why certain pneumococcal serotypes are more common in the human population.
format article
author M. Ammar Zafar
Shigeto Hamaguchi
Tonia Zangari
Michael Cammer
Jeffrey N. Weiser
author_facet M. Ammar Zafar
Shigeto Hamaguchi
Tonia Zangari
Michael Cammer
Jeffrey N. Weiser
author_sort M. Ammar Zafar
title Capsule Type and Amount Affect Shedding and Transmission of <italic toggle="yes">Streptococcus pneumoniae</italic>
title_short Capsule Type and Amount Affect Shedding and Transmission of <italic toggle="yes">Streptococcus pneumoniae</italic>
title_full Capsule Type and Amount Affect Shedding and Transmission of <italic toggle="yes">Streptococcus pneumoniae</italic>
title_fullStr Capsule Type and Amount Affect Shedding and Transmission of <italic toggle="yes">Streptococcus pneumoniae</italic>
title_full_unstemmed Capsule Type and Amount Affect Shedding and Transmission of <italic toggle="yes">Streptococcus pneumoniae</italic>
title_sort capsule type and amount affect shedding and transmission of <italic toggle="yes">streptococcus pneumoniae</italic>
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/ef71bfb9e4554d8f846479285a18232d
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