Unravelling lactate‐acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics

The d‐ and l‐forms of lactate are important fermentation metabolites produced by intestinal bacteria but are found to negatively affect mucosal barrier function and human health. Both enantiomers of lactate can be converted with acetate into the presumed beneficial butyrate by a phylogenetically rel...

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Autores principales: Shetty, Sudarshan A., Boeren, Sjef, Bui, Thi P. N., Smidt, Hauke, de Vos, Willem M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley & Sons, Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7702098/
https://www.ncbi.nlm.nih.gov/pubmed/33001550
http://dx.doi.org/10.1111/1462-2920.15269
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author Shetty, Sudarshan A.
Boeren, Sjef
Bui, Thi P. N.
Smidt, Hauke
de Vos, Willem M.
author_facet Shetty, Sudarshan A.
Boeren, Sjef
Bui, Thi P. N.
Smidt, Hauke
de Vos, Willem M.
author_sort Shetty, Sudarshan A.
collection PubMed
description The d‐ and l‐forms of lactate are important fermentation metabolites produced by intestinal bacteria but are found to negatively affect mucosal barrier function and human health. Both enantiomers of lactate can be converted with acetate into the presumed beneficial butyrate by a phylogenetically related group of anaerobes, including Anaerobutyricum and Anaerostipes spp. This is a low energy yielding process with a partially unknown pathway in Anaerobutyricum and Anaerostipes spp. and hence, we sought to address this via a comparative genomics, proteomics and physiology approach. We compared growth of Anaerobutyricum soehngenii on lactate with that on sucrose and sorbitol. Comparative proteomics revealed complete pathway of butyrate formation from sucrose, sorbitol and lactate. Notably, a gene cluster, lctABCDEF was abundantly expressed when grown on lactate. This gene cluster encodes a lactate dehydrogenase (lctD), electron transport proteins A and B (lctCB), nickel‐dependent racemase (lctE), lactate permease (lctF) and short‐chain acyl‐CoA dehydrogenase (lctG). Investigation of available genomes of intestinal bacteria revealed this new gene cluster to be highly conserved in only Anaerobutyricum and Anaerostipes spp. Present study demonstrates that A. soehngenii and several related Anaerobutyricum and Anaerostipes spp. are highly adapted for a lifestyle involving lactate plus acetate utilization in the human intestinal tract.
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spelling pubmed-77020982020-12-14 Unravelling lactate‐acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics Shetty, Sudarshan A. Boeren, Sjef Bui, Thi P. N. Smidt, Hauke de Vos, Willem M. Environ Microbiol Research Articles The d‐ and l‐forms of lactate are important fermentation metabolites produced by intestinal bacteria but are found to negatively affect mucosal barrier function and human health. Both enantiomers of lactate can be converted with acetate into the presumed beneficial butyrate by a phylogenetically related group of anaerobes, including Anaerobutyricum and Anaerostipes spp. This is a low energy yielding process with a partially unknown pathway in Anaerobutyricum and Anaerostipes spp. and hence, we sought to address this via a comparative genomics, proteomics and physiology approach. We compared growth of Anaerobutyricum soehngenii on lactate with that on sucrose and sorbitol. Comparative proteomics revealed complete pathway of butyrate formation from sucrose, sorbitol and lactate. Notably, a gene cluster, lctABCDEF was abundantly expressed when grown on lactate. This gene cluster encodes a lactate dehydrogenase (lctD), electron transport proteins A and B (lctCB), nickel‐dependent racemase (lctE), lactate permease (lctF) and short‐chain acyl‐CoA dehydrogenase (lctG). Investigation of available genomes of intestinal bacteria revealed this new gene cluster to be highly conserved in only Anaerobutyricum and Anaerostipes spp. Present study demonstrates that A. soehngenii and several related Anaerobutyricum and Anaerostipes spp. are highly adapted for a lifestyle involving lactate plus acetate utilization in the human intestinal tract. John Wiley & Sons, Inc. 2020-10-12 2020-11 /pmc/articles/PMC7702098/ /pubmed/33001550 http://dx.doi.org/10.1111/1462-2920.15269 Text en © 2020 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Shetty, Sudarshan A.
Boeren, Sjef
Bui, Thi P. N.
Smidt, Hauke
de Vos, Willem M.
Unravelling lactate‐acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics
title Unravelling lactate‐acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics
title_full Unravelling lactate‐acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics
title_fullStr Unravelling lactate‐acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics
title_full_unstemmed Unravelling lactate‐acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics
title_short Unravelling lactate‐acetate and sugar conversion into butyrate by intestinal Anaerobutyricum and Anaerostipes species by comparative proteogenomics
title_sort unravelling lactate‐acetate and sugar conversion into butyrate by intestinal anaerobutyricum and anaerostipes species by comparative proteogenomics
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7702098/
https://www.ncbi.nlm.nih.gov/pubmed/33001550
http://dx.doi.org/10.1111/1462-2920.15269
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