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Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism
Streptococcus pneumoniae is a strictly fermentative human pathogen that relies on carbohydrate metabolism to generate energy for growth. The nasopharynx colonized by the bacterium is poor in free sugars, but mucosa lining glycans can provide a source of sugar. In blood and inflamed tissues glucose i...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4595796/ https://www.ncbi.nlm.nih.gov/pubmed/26500614 http://dx.doi.org/10.3389/fmicb.2015.01041 |
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author | Paixão, Laura Caldas, José Kloosterman, Tomas G. Kuipers, Oscar P. Vinga, Susana Neves, Ana R. |
author_facet | Paixão, Laura Caldas, José Kloosterman, Tomas G. Kuipers, Oscar P. Vinga, Susana Neves, Ana R. |
author_sort | Paixão, Laura |
collection | PubMed |
description | Streptococcus pneumoniae is a strictly fermentative human pathogen that relies on carbohydrate metabolism to generate energy for growth. The nasopharynx colonized by the bacterium is poor in free sugars, but mucosa lining glycans can provide a source of sugar. In blood and inflamed tissues glucose is the prevailing sugar. As a result during progression from colonization to disease S. pneumoniae has to cope with a pronounced shift in carbohydrate nature and availability. Thus, we set out to assess the pneumococcal response to sugars found in glycans and the influence of glucose (Glc) on this response at the transcriptional, physiological, and metabolic levels. Galactose (Gal), N-acetylglucosamine (GlcNAc), and mannose (Man) affected the expression of 8 to 14% of the genes covering cellular functions including central carbon metabolism and virulence. The pattern of end-products as monitored by in vivo (13)C-NMR is in good agreement with the fermentation profiles during growth, while the pools of phosphorylated metabolites are consistent with the type of fermentation observed (homolactic vs. mixed) and regulation at the metabolic level. Furthermore, the accumulation of α-Gal6P and Man6P indicate metabolic bottlenecks in the metabolism of Gal and Man, respectively. Glc added to cells actively metabolizing other sugar(s) was readily consumed and elicited a metabolic shift toward a homolactic profile. The transcriptional response to Glc was large (over 5% of the genome). In central carbon metabolism (most represented category), Glc exerted mostly negative regulation. The smallest response to Glc was observed on a sugar mix, suggesting that exposure to varied sugars improves the fitness of S. pneumoniae. The expression of virulence factors was negatively controlled by Glc in a sugar-dependent manner. Overall, our results shed new light on the link between carbohydrate metabolism, adaptation to host niches and virulence. |
format | Online Article Text |
id | pubmed-4595796 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-45957962015-10-23 Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism Paixão, Laura Caldas, José Kloosterman, Tomas G. Kuipers, Oscar P. Vinga, Susana Neves, Ana R. Front Microbiol Microbiology Streptococcus pneumoniae is a strictly fermentative human pathogen that relies on carbohydrate metabolism to generate energy for growth. The nasopharynx colonized by the bacterium is poor in free sugars, but mucosa lining glycans can provide a source of sugar. In blood and inflamed tissues glucose is the prevailing sugar. As a result during progression from colonization to disease S. pneumoniae has to cope with a pronounced shift in carbohydrate nature and availability. Thus, we set out to assess the pneumococcal response to sugars found in glycans and the influence of glucose (Glc) on this response at the transcriptional, physiological, and metabolic levels. Galactose (Gal), N-acetylglucosamine (GlcNAc), and mannose (Man) affected the expression of 8 to 14% of the genes covering cellular functions including central carbon metabolism and virulence. The pattern of end-products as monitored by in vivo (13)C-NMR is in good agreement with the fermentation profiles during growth, while the pools of phosphorylated metabolites are consistent with the type of fermentation observed (homolactic vs. mixed) and regulation at the metabolic level. Furthermore, the accumulation of α-Gal6P and Man6P indicate metabolic bottlenecks in the metabolism of Gal and Man, respectively. Glc added to cells actively metabolizing other sugar(s) was readily consumed and elicited a metabolic shift toward a homolactic profile. The transcriptional response to Glc was large (over 5% of the genome). In central carbon metabolism (most represented category), Glc exerted mostly negative regulation. The smallest response to Glc was observed on a sugar mix, suggesting that exposure to varied sugars improves the fitness of S. pneumoniae. The expression of virulence factors was negatively controlled by Glc in a sugar-dependent manner. Overall, our results shed new light on the link between carbohydrate metabolism, adaptation to host niches and virulence. Frontiers Media S.A. 2015-10-07 /pmc/articles/PMC4595796/ /pubmed/26500614 http://dx.doi.org/10.3389/fmicb.2015.01041 Text en Copyright © 2015 Paixão, Caldas, Kloosterman, Kuipers, Vinga and Neves. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Microbiology Paixão, Laura Caldas, José Kloosterman, Tomas G. Kuipers, Oscar P. Vinga, Susana Neves, Ana R. Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism |
title | Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism |
title_full | Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism |
title_fullStr | Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism |
title_full_unstemmed | Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism |
title_short | Transcriptional and metabolic effects of glucose on Streptococcus pneumoniae sugar metabolism |
title_sort | transcriptional and metabolic effects of glucose on streptococcus pneumoniae sugar metabolism |
topic | Microbiology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4595796/ https://www.ncbi.nlm.nih.gov/pubmed/26500614 http://dx.doi.org/10.3389/fmicb.2015.01041 |
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