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Interplay between Yersinia pestis and its flea vector in lipoate metabolism

To thrive, vector-borne pathogens must survive in the vector’s gut. How these pathogens successfully exploit this environment in time and space has not been extensively characterized. Using Yersinia pestis (the plague bacillus) and its flea vector, we developed a bioluminescence-based approach and e...

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Autores principales: Bouvenot, Typhanie, Dewitte, Amélie, Bennaceur, Nadia, Pradel, Elizabeth, Pierre, François, Bontemps-Gallo, Sébastien, Sebbane, Florent
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8182812/
https://www.ncbi.nlm.nih.gov/pubmed/33479491
http://dx.doi.org/10.1038/s41396-020-00839-0
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author Bouvenot, Typhanie
Dewitte, Amélie
Bennaceur, Nadia
Pradel, Elizabeth
Pierre, François
Bontemps-Gallo, Sébastien
Sebbane, Florent
author_facet Bouvenot, Typhanie
Dewitte, Amélie
Bennaceur, Nadia
Pradel, Elizabeth
Pierre, François
Bontemps-Gallo, Sébastien
Sebbane, Florent
author_sort Bouvenot, Typhanie
collection PubMed
description To thrive, vector-borne pathogens must survive in the vector’s gut. How these pathogens successfully exploit this environment in time and space has not been extensively characterized. Using Yersinia pestis (the plague bacillus) and its flea vector, we developed a bioluminescence-based approach and employed it to investigate the mechanisms of pathogenesis at an unprecedented level of detail. Remarkably, lipoylation of metabolic enzymes, via the biosynthesis and salvage of lipoate, increases the Y. pestis transmission rate by fleas. Interestingly, the salvage pathway’s lipoate/octanoate ligase LplA enhances the first step in lipoate biosynthesis during foregut colonization but not during midgut colonization. Lastly, Y. pestis primarily uses lipoate provided by digestive proteolysis (presumably as lipoyl peptides) rather than free lipoate in blood, which is quickly depleted by the vector. Thus, spatial and temporal factors dictate the bacterium’s lipoylation strategies during an infection, and replenishment of lipoate by digestive proteolysis in the vector might constitute an Achilles’ heel that is exploited by pathogens.
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spelling pubmed-81828122021-06-07 Interplay between Yersinia pestis and its flea vector in lipoate metabolism Bouvenot, Typhanie Dewitte, Amélie Bennaceur, Nadia Pradel, Elizabeth Pierre, François Bontemps-Gallo, Sébastien Sebbane, Florent ISME J Article To thrive, vector-borne pathogens must survive in the vector’s gut. How these pathogens successfully exploit this environment in time and space has not been extensively characterized. Using Yersinia pestis (the plague bacillus) and its flea vector, we developed a bioluminescence-based approach and employed it to investigate the mechanisms of pathogenesis at an unprecedented level of detail. Remarkably, lipoylation of metabolic enzymes, via the biosynthesis and salvage of lipoate, increases the Y. pestis transmission rate by fleas. Interestingly, the salvage pathway’s lipoate/octanoate ligase LplA enhances the first step in lipoate biosynthesis during foregut colonization but not during midgut colonization. Lastly, Y. pestis primarily uses lipoate provided by digestive proteolysis (presumably as lipoyl peptides) rather than free lipoate in blood, which is quickly depleted by the vector. Thus, spatial and temporal factors dictate the bacterium’s lipoylation strategies during an infection, and replenishment of lipoate by digestive proteolysis in the vector might constitute an Achilles’ heel that is exploited by pathogens. Nature Publishing Group UK 2021-01-21 2021-04 /pmc/articles/PMC8182812/ /pubmed/33479491 http://dx.doi.org/10.1038/s41396-020-00839-0 Text en © The Author(s) 2020 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Bouvenot, Typhanie
Dewitte, Amélie
Bennaceur, Nadia
Pradel, Elizabeth
Pierre, François
Bontemps-Gallo, Sébastien
Sebbane, Florent
Interplay between Yersinia pestis and its flea vector in lipoate metabolism
title Interplay between Yersinia pestis and its flea vector in lipoate metabolism
title_full Interplay between Yersinia pestis and its flea vector in lipoate metabolism
title_fullStr Interplay between Yersinia pestis and its flea vector in lipoate metabolism
title_full_unstemmed Interplay between Yersinia pestis and its flea vector in lipoate metabolism
title_short Interplay between Yersinia pestis and its flea vector in lipoate metabolism
title_sort interplay between yersinia pestis and its flea vector in lipoate metabolism
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8182812/
https://www.ncbi.nlm.nih.gov/pubmed/33479491
http://dx.doi.org/10.1038/s41396-020-00839-0
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