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Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs

Vibrio cholerae O1, the etiological agent of cholera, is a natural inhabitant of aquatic ecosystems. Motility is a critical element for the colonization of both the human host and its environmental reservoirs. In this study, we investigated the molecular mechanisms underlying the chemotactic respons...

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Autores principales: Reddi, Geethika, Pruss, Kali, Cottingham, Kathryn L., Taylor, Ronald K., Almagro-Moreno, Salvador
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6062102/
https://www.ncbi.nlm.nih.gov/pubmed/30048543
http://dx.doi.org/10.1371/journal.pone.0201383
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author Reddi, Geethika
Pruss, Kali
Cottingham, Kathryn L.
Taylor, Ronald K.
Almagro-Moreno, Salvador
author_facet Reddi, Geethika
Pruss, Kali
Cottingham, Kathryn L.
Taylor, Ronald K.
Almagro-Moreno, Salvador
author_sort Reddi, Geethika
collection PubMed
description Vibrio cholerae O1, the etiological agent of cholera, is a natural inhabitant of aquatic ecosystems. Motility is a critical element for the colonization of both the human host and its environmental reservoirs. In this study, we investigated the molecular mechanisms underlying the chemotactic response of V. cholerae in the presence of some of its environmental reservoirs. We found that, from the several oligosaccharides found in mucin, two specifically triggered motility of V. cholerae O1: N-acetylneuraminic acid (Neu5Ac) and N-acetylglucosamine (GlcNAc). We determined that the compounds need to be internally catabolized in order to trigger motility of V. cholerae. Interestingly, the catabolism of Neu5Ac and GlcNAc converges and the production of one molecule common to both pathways, glucosamine-6-phosphate (GlcN-6P), is essential to induce motility in the presence of both compounds. Mutants unable to produce GlcN-6P show greatly reduced motility towards mucin. Furthermore, we determined that the production of GlcN-6P is necessary to induce motility of V. cholerae in the presence of some of its environmental reservoirs such as crustaceans or cyanobacteria, revealing a molecular link between the two distinct modes of the complex life cycle of V. cholerae. Finally, cross-species comparisons revealed varied chemotactic responses towards mucin, GlcNAc, and Neu5Ac for environmental (non-pathogenic) strains of V. cholerae, clinical and environmental isolates of the human pathogens Vibrio vulnificus and Vibrio parahaemolyticus, and fish and squid isolates of the symbiotic bacterium Vibrio fischeri. The data presented here suggest nuance in convergent strategies across species of the same bacterial family for motility towards suitable substrates for colonization.
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spelling pubmed-60621022018-08-03 Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs Reddi, Geethika Pruss, Kali Cottingham, Kathryn L. Taylor, Ronald K. Almagro-Moreno, Salvador PLoS One Research Article Vibrio cholerae O1, the etiological agent of cholera, is a natural inhabitant of aquatic ecosystems. Motility is a critical element for the colonization of both the human host and its environmental reservoirs. In this study, we investigated the molecular mechanisms underlying the chemotactic response of V. cholerae in the presence of some of its environmental reservoirs. We found that, from the several oligosaccharides found in mucin, two specifically triggered motility of V. cholerae O1: N-acetylneuraminic acid (Neu5Ac) and N-acetylglucosamine (GlcNAc). We determined that the compounds need to be internally catabolized in order to trigger motility of V. cholerae. Interestingly, the catabolism of Neu5Ac and GlcNAc converges and the production of one molecule common to both pathways, glucosamine-6-phosphate (GlcN-6P), is essential to induce motility in the presence of both compounds. Mutants unable to produce GlcN-6P show greatly reduced motility towards mucin. Furthermore, we determined that the production of GlcN-6P is necessary to induce motility of V. cholerae in the presence of some of its environmental reservoirs such as crustaceans or cyanobacteria, revealing a molecular link between the two distinct modes of the complex life cycle of V. cholerae. Finally, cross-species comparisons revealed varied chemotactic responses towards mucin, GlcNAc, and Neu5Ac for environmental (non-pathogenic) strains of V. cholerae, clinical and environmental isolates of the human pathogens Vibrio vulnificus and Vibrio parahaemolyticus, and fish and squid isolates of the symbiotic bacterium Vibrio fischeri. The data presented here suggest nuance in convergent strategies across species of the same bacterial family for motility towards suitable substrates for colonization. Public Library of Science 2018-07-26 /pmc/articles/PMC6062102/ /pubmed/30048543 http://dx.doi.org/10.1371/journal.pone.0201383 Text en © 2018 Reddi 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 (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Reddi, Geethika
Pruss, Kali
Cottingham, Kathryn L.
Taylor, Ronald K.
Almagro-Moreno, Salvador
Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs
title Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs
title_full Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs
title_fullStr Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs
title_full_unstemmed Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs
title_short Catabolism of mucus components influences motility of Vibrio cholerae in the presence of environmental reservoirs
title_sort catabolism of mucus components influences motility of vibrio cholerae in the presence of environmental reservoirs
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6062102/
https://www.ncbi.nlm.nih.gov/pubmed/30048543
http://dx.doi.org/10.1371/journal.pone.0201383
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