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Formate simultaneously reduces oxidase activity and enhances respiration in Campylobacter jejuni

The foodborne microaerophilic pathogen, Campylobacter jejuni, possesses a periplasmic formate dehydrogenase and two terminal oxidases, which serve to metabolize formate and facilitate the use of oxygen as a terminal electron acceptor, respectively. Formate, a primary energy source for C. jejuni, inh...

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Autores principales: Kassem, Issmat I., Candelero-Rueda, Rosario A., Esseili, Kawthar A., Rajashekara, Gireesh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5238407/
https://www.ncbi.nlm.nih.gov/pubmed/28091524
http://dx.doi.org/10.1038/srep40117
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author Kassem, Issmat I.
Candelero-Rueda, Rosario A.
Esseili, Kawthar A.
Rajashekara, Gireesh
author_facet Kassem, Issmat I.
Candelero-Rueda, Rosario A.
Esseili, Kawthar A.
Rajashekara, Gireesh
author_sort Kassem, Issmat I.
collection PubMed
description The foodborne microaerophilic pathogen, Campylobacter jejuni, possesses a periplasmic formate dehydrogenase and two terminal oxidases, which serve to metabolize formate and facilitate the use of oxygen as a terminal electron acceptor, respectively. Formate, a primary energy source for C. jejuni, inhibits oxidase activity in other bacteria. Here, we hypothesized that formate might affect both energy metabolism and microaerobic survival in C. jejuni. Subsequently, we showed that C. jejuni 81–176 (wildtype) exhibited enhanced chemoattraction to and respiration of formate in comparison to other organic acids. Formate also significantly increased C. jejuni’s growth, motility, and biofilm formation under microaerobic (5% O(2)) conditions. However, formate reduced oxidase activity under microaerobic conditions as well as aerotolerance and biofilm formation under ambient oxygen conditions. The expression of genes encoding the ribonucleotide reductase (RNR) and proteins that facilitate the use of alternative electron acceptors generally increased in the presence of formate. Taken together, formate might play a role in optimizing C. jejuni’s adaptation to the oxygen-limited gastrointestinal tract of the host. By affecting oxidase activity, formate possibly facilitates shuttling electrons to alternative acceptors, while likely conserving limited oxygen concentrations for other essential functions such as DNA synthesis via RNR which is required for C. jejuni’s growth.
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spelling pubmed-52384072017-01-19 Formate simultaneously reduces oxidase activity and enhances respiration in Campylobacter jejuni Kassem, Issmat I. Candelero-Rueda, Rosario A. Esseili, Kawthar A. Rajashekara, Gireesh Sci Rep Article The foodborne microaerophilic pathogen, Campylobacter jejuni, possesses a periplasmic formate dehydrogenase and two terminal oxidases, which serve to metabolize formate and facilitate the use of oxygen as a terminal electron acceptor, respectively. Formate, a primary energy source for C. jejuni, inhibits oxidase activity in other bacteria. Here, we hypothesized that formate might affect both energy metabolism and microaerobic survival in C. jejuni. Subsequently, we showed that C. jejuni 81–176 (wildtype) exhibited enhanced chemoattraction to and respiration of formate in comparison to other organic acids. Formate also significantly increased C. jejuni’s growth, motility, and biofilm formation under microaerobic (5% O(2)) conditions. However, formate reduced oxidase activity under microaerobic conditions as well as aerotolerance and biofilm formation under ambient oxygen conditions. The expression of genes encoding the ribonucleotide reductase (RNR) and proteins that facilitate the use of alternative electron acceptors generally increased in the presence of formate. Taken together, formate might play a role in optimizing C. jejuni’s adaptation to the oxygen-limited gastrointestinal tract of the host. By affecting oxidase activity, formate possibly facilitates shuttling electrons to alternative acceptors, while likely conserving limited oxygen concentrations for other essential functions such as DNA synthesis via RNR which is required for C. jejuni’s growth. Nature Publishing Group 2017-01-16 /pmc/articles/PMC5238407/ /pubmed/28091524 http://dx.doi.org/10.1038/srep40117 Text en Copyright © 2017, The Author(s) http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Kassem, Issmat I.
Candelero-Rueda, Rosario A.
Esseili, Kawthar A.
Rajashekara, Gireesh
Formate simultaneously reduces oxidase activity and enhances respiration in Campylobacter jejuni
title Formate simultaneously reduces oxidase activity and enhances respiration in Campylobacter jejuni
title_full Formate simultaneously reduces oxidase activity and enhances respiration in Campylobacter jejuni
title_fullStr Formate simultaneously reduces oxidase activity and enhances respiration in Campylobacter jejuni
title_full_unstemmed Formate simultaneously reduces oxidase activity and enhances respiration in Campylobacter jejuni
title_short Formate simultaneously reduces oxidase activity and enhances respiration in Campylobacter jejuni
title_sort formate simultaneously reduces oxidase activity and enhances respiration in campylobacter jejuni
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5238407/
https://www.ncbi.nlm.nih.gov/pubmed/28091524
http://dx.doi.org/10.1038/srep40117
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