Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation

The composition of gut-associated microbial communities changes during intestinal inflammation, including an expansion of Enterobacteriaceae populations. The mechanisms underlying microbiota changes during inflammation are incompletely understood. Here, we analyzed previously published metagenomic d...

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Autores principales: Elizabeth R Hughes, Maria G Winter, Laice Alves da Silva, Matthew K Muramatsu, Angel G Jimenez, Caroline C Gillis, Luisella Spiga, Rachael B Chanin, Renato L Santos, Wenhan Zhu, Sebastian E Winter
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Publicado: eLife Sciences Publications Ltd 2021
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Acceso en línea:https://doaj.org/article/fd14f6f2f03b419ba41300000a9ffb71
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spelling oai:doaj.org-article:fd14f6f2f03b419ba41300000a9ffb712021-11-11T09:31:34ZReshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation10.7554/eLife.586092050-084Xe58609https://doaj.org/article/fd14f6f2f03b419ba41300000a9ffb712021-06-01T00:00:00Zhttps://elifesciences.org/articles/58609https://doaj.org/toc/2050-084XThe composition of gut-associated microbial communities changes during intestinal inflammation, including an expansion of Enterobacteriaceae populations. The mechanisms underlying microbiota changes during inflammation are incompletely understood. Here, we analyzed previously published metagenomic datasets with a focus on microbial hydrogen metabolism. The bacterial genomes in the inflamed murine gut and in patients with inflammatory bowel disease contained more genes encoding predicted hydrogen-utilizing hydrogenases compared to communities found under non-inflamed conditions. To validate these findings, we investigated hydrogen metabolism of Escherichia coli, a representative Enterobacteriaceae, in mouse models of colitis. E. coli mutants lacking hydrogenase-1 and hydrogenase-2 displayed decreased fitness during colonization of the inflamed cecum and colon. Utilization of molecular hydrogen was in part dependent on respiration of inflammation-derived electron acceptors. This work highlights the contribution of hydrogenases to alterations of the gut microbiota in the context of non-infectious colitis.Elizabeth R HughesMaria G WinterLaice Alves da SilvaMatthew K MuramatsuAngel G JimenezCaroline C GillisLuisella SpigaRachael B ChaninRenato L SantosWenhan ZhuSebastian E WintereLife Sciences Publications Ltdarticlegut microbiotadysbiosisintestinal inflammationhydrogenasemolecular hydrogenMedicineRScienceQBiology (General)QH301-705.5ENeLife, Vol 10 (2021)
institution DOAJ
collection DOAJ
language EN
topic gut microbiota
dysbiosis
intestinal inflammation
hydrogenase
molecular hydrogen
Medicine
R
Science
Q
Biology (General)
QH301-705.5
spellingShingle gut microbiota
dysbiosis
intestinal inflammation
hydrogenase
molecular hydrogen
Medicine
R
Science
Q
Biology (General)
QH301-705.5
Elizabeth R Hughes
Maria G Winter
Laice Alves da Silva
Matthew K Muramatsu
Angel G Jimenez
Caroline C Gillis
Luisella Spiga
Rachael B Chanin
Renato L Santos
Wenhan Zhu
Sebastian E Winter
Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation
description The composition of gut-associated microbial communities changes during intestinal inflammation, including an expansion of Enterobacteriaceae populations. The mechanisms underlying microbiota changes during inflammation are incompletely understood. Here, we analyzed previously published metagenomic datasets with a focus on microbial hydrogen metabolism. The bacterial genomes in the inflamed murine gut and in patients with inflammatory bowel disease contained more genes encoding predicted hydrogen-utilizing hydrogenases compared to communities found under non-inflamed conditions. To validate these findings, we investigated hydrogen metabolism of Escherichia coli, a representative Enterobacteriaceae, in mouse models of colitis. E. coli mutants lacking hydrogenase-1 and hydrogenase-2 displayed decreased fitness during colonization of the inflamed cecum and colon. Utilization of molecular hydrogen was in part dependent on respiration of inflammation-derived electron acceptors. This work highlights the contribution of hydrogenases to alterations of the gut microbiota in the context of non-infectious colitis.
format article
author Elizabeth R Hughes
Maria G Winter
Laice Alves da Silva
Matthew K Muramatsu
Angel G Jimenez
Caroline C Gillis
Luisella Spiga
Rachael B Chanin
Renato L Santos
Wenhan Zhu
Sebastian E Winter
author_facet Elizabeth R Hughes
Maria G Winter
Laice Alves da Silva
Matthew K Muramatsu
Angel G Jimenez
Caroline C Gillis
Luisella Spiga
Rachael B Chanin
Renato L Santos
Wenhan Zhu
Sebastian E Winter
author_sort Elizabeth R Hughes
title Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation
title_short Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation
title_full Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation
title_fullStr Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation
title_full_unstemmed Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammation
title_sort reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal e. coli during gut inflammation
publisher eLife Sciences Publications Ltd
publishDate 2021
url https://doaj.org/article/fd14f6f2f03b419ba41300000a9ffb71
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