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...
| Main Authors: | , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2021-06-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/58609 |
| _version_ | 1811180388728438784 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-11T09:02:18Z |
| format | Article |
| id | doaj.art-fd14f6f2f03b419ba41300000a9ffb71 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:02:18Z |
| publishDate | 2021-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-fd14f6f2f03b419ba41300000a9ffb712022-12-22T04:32:45ZengeLife Sciences Publications LtdeLife2050-084X2021-06-011010.7554/eLife.58609Reshaping of bacterial molecular hydrogen metabolism contributes to the outgrowth of commensal E. coli during gut inflammationElizabeth R Hughes0https://orcid.org/0000-0003-4967-8819Maria G Winter1Laice Alves da Silva2Matthew K Muramatsu3Angel G Jimenez4Caroline C Gillis5Luisella Spiga6Rachael B Chanin7Renato L Santos8Wenhan Zhu9Sebastian E Winter10https://orcid.org/0000-0003-1532-9178Department of Microbiology, UT Southwestern, Dallas, United StatesDepartment of Microbiology, UT Southwestern, Dallas, United StatesDepartamento de Clinica e Cirurgia Veterinarias, Escola de Veterinaria, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartment of Microbiology, UT Southwestern, Dallas, United StatesDepartment of Microbiology, UT Southwestern, Dallas, United StatesDepartment of Microbiology, UT Southwestern, Dallas, United StatesDepartment of Microbiology, UT Southwestern, Dallas, United StatesDepartment of Microbiology, UT Southwestern, Dallas, United StatesDepartamento de Clinica e Cirurgia Veterinarias, Escola de Veterinaria, Universidade Federal de Minas Gerais, Belo Horizonte, BrazilDepartment of Microbiology, UT Southwestern, Dallas, United StatesDepartment of Microbiology, UT Southwestern, Dallas, United States; Department of Immunology, UT Southwestern, Dallas, United StatesThe 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.https://elifesciences.org/articles/58609gut microbiotadysbiosisintestinal inflammationhydrogenasemolecular hydrogen |
| spellingShingle | 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 eLife gut microbiota dysbiosis intestinal inflammation hydrogenase molecular hydrogen |
| title | 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_short | 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 |
| topic | gut microbiota dysbiosis intestinal inflammation hydrogenase molecular hydrogen |
| url | https://elifesciences.org/articles/58609 |
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