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Capsule Type of Streptococcus pneumoniae Determines Growth Phenotype
The polysaccharide capsule of Streptococcus pneumoniae defines over ninety serotypes, which differ in their carriage prevalence and invasiveness for poorly understood reasons. Recently, an inverse correlation between carriage prevalence and oligosaccharide structure of a given capsule has been descr...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2012
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3297593/ https://www.ncbi.nlm.nih.gov/pubmed/22412375 http://dx.doi.org/10.1371/journal.ppat.1002574 |
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author | Hathaway, Lucy J. Brugger, Silvio D. Morand, Brigitte Bangert, Mathieu Rotzetter, Jeannine U. Hauser, Christoph Graber, Werner A. Gore, Suzanna Kadioglu, Aras Mühlemann, Kathrin |
author_facet | Hathaway, Lucy J. Brugger, Silvio D. Morand, Brigitte Bangert, Mathieu Rotzetter, Jeannine U. Hauser, Christoph Graber, Werner A. Gore, Suzanna Kadioglu, Aras Mühlemann, Kathrin |
author_sort | Hathaway, Lucy J. |
collection | PubMed |
description | The polysaccharide capsule of Streptococcus pneumoniae defines over ninety serotypes, which differ in their carriage prevalence and invasiveness for poorly understood reasons. Recently, an inverse correlation between carriage prevalence and oligosaccharide structure of a given capsule has been described. Our previous work suggested a link between serotype and growth in vitro. Here we investigate whether capsule production interferes with growth in vitro and whether this predicts carriage prevalence in vivo. Eighty-one capsule switch mutants were constructed representing nine different serotypes, five of low (4, 7F, 14, 15, 18C) and four of high carriage prevalence (6B, 9V, 19F, 23F). Growth (length of lag phase, maximum optical density) of wildtype strains, nontypeable mutants and capsule switch mutants was studied in nutrient-restricted Lacks medium (MLM) and in rich undefined brain heart infusion broth supplemented with 5% foetal calf serum (BHI+FCS). In MLM growth phenotype depended on, and was transferred with, capsule operon type. Colonization efficiency of mouse nasopharynx also depended on, and was transferred with, capsule operon type. Capsule production interfered with growth, which correlated inversely with serotype-specific carriage prevalence. Serotypes with better growth and higher carriage prevalence produced thicker capsules (by electron microscopy, FITC-dextran exclusion assays and HPLC) than serotypes with delayed growth and low carriage prevalence. However, expression of cpsA, the first capsule gene, (by quantitative RT-PCR) correlated inversely with capsule thickness. Energy spent for capsule production (incorporation of H3-glucose) relative to amount of capsule produced was higher for serotypes with low carriage prevalence. Experiments in BHI+FCS showed overall better bacterial growth and more capsule production than growth in MLM and differences between serotypes were no longer apparent. Production of polysaccharide capsule in S. pneumoniae interferes with growth in nutrient-limiting conditions probably by competition for energy against the central metabolism. Serotype-specific nasopharyngeal carriage prevalence in vivo is predicted by the growth phenotype. |
format | Online Article Text |
id | pubmed-3297593 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2012 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-32975932012-03-12 Capsule Type of Streptococcus pneumoniae Determines Growth Phenotype Hathaway, Lucy J. Brugger, Silvio D. Morand, Brigitte Bangert, Mathieu Rotzetter, Jeannine U. Hauser, Christoph Graber, Werner A. Gore, Suzanna Kadioglu, Aras Mühlemann, Kathrin PLoS Pathog Research Article The polysaccharide capsule of Streptococcus pneumoniae defines over ninety serotypes, which differ in their carriage prevalence and invasiveness for poorly understood reasons. Recently, an inverse correlation between carriage prevalence and oligosaccharide structure of a given capsule has been described. Our previous work suggested a link between serotype and growth in vitro. Here we investigate whether capsule production interferes with growth in vitro and whether this predicts carriage prevalence in vivo. Eighty-one capsule switch mutants were constructed representing nine different serotypes, five of low (4, 7F, 14, 15, 18C) and four of high carriage prevalence (6B, 9V, 19F, 23F). Growth (length of lag phase, maximum optical density) of wildtype strains, nontypeable mutants and capsule switch mutants was studied in nutrient-restricted Lacks medium (MLM) and in rich undefined brain heart infusion broth supplemented with 5% foetal calf serum (BHI+FCS). In MLM growth phenotype depended on, and was transferred with, capsule operon type. Colonization efficiency of mouse nasopharynx also depended on, and was transferred with, capsule operon type. Capsule production interfered with growth, which correlated inversely with serotype-specific carriage prevalence. Serotypes with better growth and higher carriage prevalence produced thicker capsules (by electron microscopy, FITC-dextran exclusion assays and HPLC) than serotypes with delayed growth and low carriage prevalence. However, expression of cpsA, the first capsule gene, (by quantitative RT-PCR) correlated inversely with capsule thickness. Energy spent for capsule production (incorporation of H3-glucose) relative to amount of capsule produced was higher for serotypes with low carriage prevalence. Experiments in BHI+FCS showed overall better bacterial growth and more capsule production than growth in MLM and differences between serotypes were no longer apparent. Production of polysaccharide capsule in S. pneumoniae interferes with growth in nutrient-limiting conditions probably by competition for energy against the central metabolism. Serotype-specific nasopharyngeal carriage prevalence in vivo is predicted by the growth phenotype. Public Library of Science 2012-03-08 /pmc/articles/PMC3297593/ /pubmed/22412375 http://dx.doi.org/10.1371/journal.ppat.1002574 Text en Hathaway et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Hathaway, Lucy J. Brugger, Silvio D. Morand, Brigitte Bangert, Mathieu Rotzetter, Jeannine U. Hauser, Christoph Graber, Werner A. Gore, Suzanna Kadioglu, Aras Mühlemann, Kathrin Capsule Type of Streptococcus pneumoniae Determines Growth Phenotype |
title | Capsule Type of Streptococcus pneumoniae Determines Growth Phenotype |
title_full | Capsule Type of Streptococcus pneumoniae Determines Growth Phenotype |
title_fullStr | Capsule Type of Streptococcus pneumoniae Determines Growth Phenotype |
title_full_unstemmed | Capsule Type of Streptococcus pneumoniae Determines Growth Phenotype |
title_short | Capsule Type of Streptococcus pneumoniae Determines Growth Phenotype |
title_sort | capsule type of streptococcus pneumoniae determines growth phenotype |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3297593/ https://www.ncbi.nlm.nih.gov/pubmed/22412375 http://dx.doi.org/10.1371/journal.ppat.1002574 |
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