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Common Cell Shape Evolution of Two Nasopharyngeal Pathogens

Respiratory infectious diseases are the third cause of worldwide death. The nasopharynx is the portal of entry and the ecological niche of many microorganisms, of which some are pathogenic to humans, such as Neisseria meningitidis and Moraxella catarrhalis. These microbes possess several surface str...

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Autores principales: Veyrier, Frédéric J., Biais, Nicolas, Morales, Pablo, Belkacem, Nouria, Guilhen, Cyril, Ranjeva, Sylvia, Sismeiro, Odile, Péhau-Arnaudet, Gérard, Rocha, Eduardo P., Werts, Catherine, Taha, Muhamed-Kheir, Boneca, Ivo G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4498754/
https://www.ncbi.nlm.nih.gov/pubmed/26162030
http://dx.doi.org/10.1371/journal.pgen.1005338
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author Veyrier, Frédéric J.
Biais, Nicolas
Morales, Pablo
Belkacem, Nouria
Guilhen, Cyril
Ranjeva, Sylvia
Sismeiro, Odile
Péhau-Arnaudet, Gérard
Rocha, Eduardo P.
Werts, Catherine
Taha, Muhamed-Kheir
Boneca, Ivo G.
author_facet Veyrier, Frédéric J.
Biais, Nicolas
Morales, Pablo
Belkacem, Nouria
Guilhen, Cyril
Ranjeva, Sylvia
Sismeiro, Odile
Péhau-Arnaudet, Gérard
Rocha, Eduardo P.
Werts, Catherine
Taha, Muhamed-Kheir
Boneca, Ivo G.
author_sort Veyrier, Frédéric J.
collection PubMed
description Respiratory infectious diseases are the third cause of worldwide death. The nasopharynx is the portal of entry and the ecological niche of many microorganisms, of which some are pathogenic to humans, such as Neisseria meningitidis and Moraxella catarrhalis. These microbes possess several surface structures that interact with the actors of the innate immune system. In our attempt to understand the past evolution of these bacteria and their adaption to the nasopharynx, we first studied differences in cell wall structure, one of the strongest immune-modulators. We were able to show that a modification of peptidoglycan (PG) composition (increased proportion of pentapeptides) and a cell shape change from rod to cocci had been selected for along the past evolution of N. meningitidis. Using genomic comparison across species, we correlated the emergence of the new cell shape (cocci) with the deletion, from the genome of N. meningitidis ancestor, of only one gene: yacF. Moreover, the reconstruction of this genetic deletion in a bacterium harboring the ancestral version of the locus together with the analysis of the PG structure, suggest that this gene is coordinating the transition from cell elongation to cell division. Accompanying the loss of yacF, the elongation machinery was also lost by several of the descendants leading to the change in the PG structure observed in N. meningitidis. Finally, the same evolution was observed for the ancestor of M. catarrhalis. This suggests a strong selection of these genetic events during the colonization of the nasopharynx. This selection may have been forced by the requirement of evolving permissive interaction with the immune system, the need to reduce the cellular surface exposed to immune attacks without reducing the intracellular storage capacity, or the necessity to better compete for adhesion to target cells.
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spelling pubmed-44987542015-07-17 Common Cell Shape Evolution of Two Nasopharyngeal Pathogens Veyrier, Frédéric J. Biais, Nicolas Morales, Pablo Belkacem, Nouria Guilhen, Cyril Ranjeva, Sylvia Sismeiro, Odile Péhau-Arnaudet, Gérard Rocha, Eduardo P. Werts, Catherine Taha, Muhamed-Kheir Boneca, Ivo G. PLoS Genet Research Article Respiratory infectious diseases are the third cause of worldwide death. The nasopharynx is the portal of entry and the ecological niche of many microorganisms, of which some are pathogenic to humans, such as Neisseria meningitidis and Moraxella catarrhalis. These microbes possess several surface structures that interact with the actors of the innate immune system. In our attempt to understand the past evolution of these bacteria and their adaption to the nasopharynx, we first studied differences in cell wall structure, one of the strongest immune-modulators. We were able to show that a modification of peptidoglycan (PG) composition (increased proportion of pentapeptides) and a cell shape change from rod to cocci had been selected for along the past evolution of N. meningitidis. Using genomic comparison across species, we correlated the emergence of the new cell shape (cocci) with the deletion, from the genome of N. meningitidis ancestor, of only one gene: yacF. Moreover, the reconstruction of this genetic deletion in a bacterium harboring the ancestral version of the locus together with the analysis of the PG structure, suggest that this gene is coordinating the transition from cell elongation to cell division. Accompanying the loss of yacF, the elongation machinery was also lost by several of the descendants leading to the change in the PG structure observed in N. meningitidis. Finally, the same evolution was observed for the ancestor of M. catarrhalis. This suggests a strong selection of these genetic events during the colonization of the nasopharynx. This selection may have been forced by the requirement of evolving permissive interaction with the immune system, the need to reduce the cellular surface exposed to immune attacks without reducing the intracellular storage capacity, or the necessity to better compete for adhesion to target cells. Public Library of Science 2015-07-10 /pmc/articles/PMC4498754/ /pubmed/26162030 http://dx.doi.org/10.1371/journal.pgen.1005338 Text en © 2015 Veyrier 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
Veyrier, Frédéric J.
Biais, Nicolas
Morales, Pablo
Belkacem, Nouria
Guilhen, Cyril
Ranjeva, Sylvia
Sismeiro, Odile
Péhau-Arnaudet, Gérard
Rocha, Eduardo P.
Werts, Catherine
Taha, Muhamed-Kheir
Boneca, Ivo G.
Common Cell Shape Evolution of Two Nasopharyngeal Pathogens
title Common Cell Shape Evolution of Two Nasopharyngeal Pathogens
title_full Common Cell Shape Evolution of Two Nasopharyngeal Pathogens
title_fullStr Common Cell Shape Evolution of Two Nasopharyngeal Pathogens
title_full_unstemmed Common Cell Shape Evolution of Two Nasopharyngeal Pathogens
title_short Common Cell Shape Evolution of Two Nasopharyngeal Pathogens
title_sort common cell shape evolution of two nasopharyngeal pathogens
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4498754/
https://www.ncbi.nlm.nih.gov/pubmed/26162030
http://dx.doi.org/10.1371/journal.pgen.1005338
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