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Autoinducer 2 Signaling via the Phosphotransferase FruA Drives Galactose Utilization by Streptococcus pneumoniae, Resulting in Hypervirulence

Communication between bacterial cells is crucial for the coordination of diverse cellular processes that facilitate environmental adaptation and, in the case of pathogenic species, virulence. This is achieved by the secretion and detection of small signaling molecules called autoinducers, a process...

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Autores principales: Trappetti, Claudia, McAllister, Lauren J., Chen, Austen, Wang, Hui, Paton, Adrienne W., Oggioni, Marco R., McDevitt, Christopher A., Paton, James C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5263250/
https://www.ncbi.nlm.nih.gov/pubmed/28119473
http://dx.doi.org/10.1128/mBio.02269-16
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author Trappetti, Claudia
McAllister, Lauren J.
Chen, Austen
Wang, Hui
Paton, Adrienne W.
Oggioni, Marco R.
McDevitt, Christopher A.
Paton, James C.
author_facet Trappetti, Claudia
McAllister, Lauren J.
Chen, Austen
Wang, Hui
Paton, Adrienne W.
Oggioni, Marco R.
McDevitt, Christopher A.
Paton, James C.
author_sort Trappetti, Claudia
collection PubMed
description Communication between bacterial cells is crucial for the coordination of diverse cellular processes that facilitate environmental adaptation and, in the case of pathogenic species, virulence. This is achieved by the secretion and detection of small signaling molecules called autoinducers, a process termed quorum sensing. To date, the only signaling molecule recognized by both Gram-positive and Gram-negative bacteria is autoinducer 2 (AI-2), synthesized by the metabolic enzyme LuxS (S-ribosylhomocysteine lyase) as a by-product of the activated methyl cycle. Homologues of LuxS are ubiquitous in bacteria, suggesting a key role in interspecies, as well as intraspecies, communication. Gram-negative bacteria sense and respond to AI-2 via the Lsr ABC transporter system or by the LuxP/LuxQ phosphorelay system. However, homologues of these systems are absent from Gram-positive bacteria and the AI-2 receptor is unknown. Here we show that in the major human pathogen Streptococcus pneumoniae, sensing of exogenous AI-2 is dependent on FruA, a fructose-specific phosphoenolpyruvate-phosphotransferase system that is highly conserved in Gram-positive pathogens. Importantly, AI-2 signaling via FruA enables the bacterium to utilize galactose as a carbon source and upregulates the Leloir pathway, thereby leading to increased production of capsular polysaccharide and a hypervirulent phenotype.
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spelling pubmed-52632502017-01-25 Autoinducer 2 Signaling via the Phosphotransferase FruA Drives Galactose Utilization by Streptococcus pneumoniae, Resulting in Hypervirulence Trappetti, Claudia McAllister, Lauren J. Chen, Austen Wang, Hui Paton, Adrienne W. Oggioni, Marco R. McDevitt, Christopher A. Paton, James C. mBio Research Article Communication between bacterial cells is crucial for the coordination of diverse cellular processes that facilitate environmental adaptation and, in the case of pathogenic species, virulence. This is achieved by the secretion and detection of small signaling molecules called autoinducers, a process termed quorum sensing. To date, the only signaling molecule recognized by both Gram-positive and Gram-negative bacteria is autoinducer 2 (AI-2), synthesized by the metabolic enzyme LuxS (S-ribosylhomocysteine lyase) as a by-product of the activated methyl cycle. Homologues of LuxS are ubiquitous in bacteria, suggesting a key role in interspecies, as well as intraspecies, communication. Gram-negative bacteria sense and respond to AI-2 via the Lsr ABC transporter system or by the LuxP/LuxQ phosphorelay system. However, homologues of these systems are absent from Gram-positive bacteria and the AI-2 receptor is unknown. Here we show that in the major human pathogen Streptococcus pneumoniae, sensing of exogenous AI-2 is dependent on FruA, a fructose-specific phosphoenolpyruvate-phosphotransferase system that is highly conserved in Gram-positive pathogens. Importantly, AI-2 signaling via FruA enables the bacterium to utilize galactose as a carbon source and upregulates the Leloir pathway, thereby leading to increased production of capsular polysaccharide and a hypervirulent phenotype. American Society for Microbiology 2017-01-24 /pmc/articles/PMC5263250/ /pubmed/28119473 http://dx.doi.org/10.1128/mBio.02269-16 Text en Copyright © 2017 Trappetti et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Trappetti, Claudia
McAllister, Lauren J.
Chen, Austen
Wang, Hui
Paton, Adrienne W.
Oggioni, Marco R.
McDevitt, Christopher A.
Paton, James C.
Autoinducer 2 Signaling via the Phosphotransferase FruA Drives Galactose Utilization by Streptococcus pneumoniae, Resulting in Hypervirulence
title Autoinducer 2 Signaling via the Phosphotransferase FruA Drives Galactose Utilization by Streptococcus pneumoniae, Resulting in Hypervirulence
title_full Autoinducer 2 Signaling via the Phosphotransferase FruA Drives Galactose Utilization by Streptococcus pneumoniae, Resulting in Hypervirulence
title_fullStr Autoinducer 2 Signaling via the Phosphotransferase FruA Drives Galactose Utilization by Streptococcus pneumoniae, Resulting in Hypervirulence
title_full_unstemmed Autoinducer 2 Signaling via the Phosphotransferase FruA Drives Galactose Utilization by Streptococcus pneumoniae, Resulting in Hypervirulence
title_short Autoinducer 2 Signaling via the Phosphotransferase FruA Drives Galactose Utilization by Streptococcus pneumoniae, Resulting in Hypervirulence
title_sort autoinducer 2 signaling via the phosphotransferase frua drives galactose utilization by streptococcus pneumoniae, resulting in hypervirulence
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5263250/
https://www.ncbi.nlm.nih.gov/pubmed/28119473
http://dx.doi.org/10.1128/mBio.02269-16
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