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Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity

Campylobacter concisus is an emerging enteric pathogen that is associated with inflammatory bowel disease. Previous studies demonstrated that C. concisus is non-saccharolytic and hydrogen gas (H(2)) is a critical factor for C. concisus growth. In order to understand the molecular basis of the non-sa...

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Autores principales: Yeow, Melissa, Liu, Fang, Ma, Rena, Williams, Timothy J., Riordan, Stephen M., Zhang, Li
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7059363/
https://www.ncbi.nlm.nih.gov/pubmed/32165925
http://dx.doi.org/10.1186/s13099-020-00349-6
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author Yeow, Melissa
Liu, Fang
Ma, Rena
Williams, Timothy J.
Riordan, Stephen M.
Zhang, Li
author_facet Yeow, Melissa
Liu, Fang
Ma, Rena
Williams, Timothy J.
Riordan, Stephen M.
Zhang, Li
author_sort Yeow, Melissa
collection PubMed
description Campylobacter concisus is an emerging enteric pathogen that is associated with inflammatory bowel disease. Previous studies demonstrated that C. concisus is non-saccharolytic and hydrogen gas (H(2)) is a critical factor for C. concisus growth. In order to understand the molecular basis of the non-saccharolytic and H(2)-dependent nature of C. concisus growth, in this study we examined the pathways involving energy metabolism and oxidative stress defence in C. concisus. Bioinformatic analysis of C. concisus genomes in comparison with the well-studied enteric pathogen Campylobacter jejuni was performed. This study found that C. concisus lacks a number of key enzymes in glycolysis, including glucokinase and phosphofructokinase, and the oxidative pentose phosphate pathway. C. concisus has an incomplete tricarboxylic acid cycle, with no identifiable succinyl-CoA synthase or fumarate hydratase. C. concisus was inferred to use fewer amino acids and have fewer candidate substrates as electron donors and acceptors compared to C. jejuni. The addition of DMSO or fumarate to media resulted in significantly increased growth of C. concisus in the presence of H(2) as an electron donor, demonstrating that both can be used as electron acceptors. Catalase, an essential enzyme for oxidative stress defence in C. jejuni, and various nitrosative stress enzymes, were not found in the C. concisus genome. Overall, C. concisus is inferred to have a non-saccharolytic metabolism in which H(2) is central to energy conservation, and a narrow selection of carboxylic acids and amino acids can be utilised as organic substrates. In conclusion, this study provides a molecular basis for the non-saccharolytic and hydrogen-dependent nature of C. concisus energy metabolism pathways, which provides insights into the growth requirements and pathogenicity of this species.
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spelling pubmed-70593632020-03-12 Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity Yeow, Melissa Liu, Fang Ma, Rena Williams, Timothy J. Riordan, Stephen M. Zhang, Li Gut Pathog Research Campylobacter concisus is an emerging enteric pathogen that is associated with inflammatory bowel disease. Previous studies demonstrated that C. concisus is non-saccharolytic and hydrogen gas (H(2)) is a critical factor for C. concisus growth. In order to understand the molecular basis of the non-saccharolytic and H(2)-dependent nature of C. concisus growth, in this study we examined the pathways involving energy metabolism and oxidative stress defence in C. concisus. Bioinformatic analysis of C. concisus genomes in comparison with the well-studied enteric pathogen Campylobacter jejuni was performed. This study found that C. concisus lacks a number of key enzymes in glycolysis, including glucokinase and phosphofructokinase, and the oxidative pentose phosphate pathway. C. concisus has an incomplete tricarboxylic acid cycle, with no identifiable succinyl-CoA synthase or fumarate hydratase. C. concisus was inferred to use fewer amino acids and have fewer candidate substrates as electron donors and acceptors compared to C. jejuni. The addition of DMSO or fumarate to media resulted in significantly increased growth of C. concisus in the presence of H(2) as an electron donor, demonstrating that both can be used as electron acceptors. Catalase, an essential enzyme for oxidative stress defence in C. jejuni, and various nitrosative stress enzymes, were not found in the C. concisus genome. Overall, C. concisus is inferred to have a non-saccharolytic metabolism in which H(2) is central to energy conservation, and a narrow selection of carboxylic acids and amino acids can be utilised as organic substrates. In conclusion, this study provides a molecular basis for the non-saccharolytic and hydrogen-dependent nature of C. concisus energy metabolism pathways, which provides insights into the growth requirements and pathogenicity of this species. BioMed Central 2020-03-05 /pmc/articles/PMC7059363/ /pubmed/32165925 http://dx.doi.org/10.1186/s13099-020-00349-6 Text en © The Author(s) 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Yeow, Melissa
Liu, Fang
Ma, Rena
Williams, Timothy J.
Riordan, Stephen M.
Zhang, Li
Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity
title Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity
title_full Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity
title_fullStr Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity
title_full_unstemmed Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity
title_short Analyses of energy metabolism and stress defence provide insights into Campylobacter concisus growth and pathogenicity
title_sort analyses of energy metabolism and stress defence provide insights into campylobacter concisus growth and pathogenicity
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7059363/
https://www.ncbi.nlm.nih.gov/pubmed/32165925
http://dx.doi.org/10.1186/s13099-020-00349-6
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