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Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron

A large variety of microbes are present in the human gut, some of which are considered to interact with each other. Most of these interactions involve bacterial metabolites. Phascolarctobacterium faecium hardly uses carbohydrates for growth and instead uses succinate as a substrate. This study inves...

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Autores principales: Ikeyama, Nao, Murakami, Takumi, Toyoda, Atsushi, Mori, Hiroshi, Iino, Takao, Ohkuma, Moriya, Sakamoto, Mitsuo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7568257/
https://www.ncbi.nlm.nih.gov/pubmed/32856395
http://dx.doi.org/10.1002/mbo3.1111
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author Ikeyama, Nao
Murakami, Takumi
Toyoda, Atsushi
Mori, Hiroshi
Iino, Takao
Ohkuma, Moriya
Sakamoto, Mitsuo
author_facet Ikeyama, Nao
Murakami, Takumi
Toyoda, Atsushi
Mori, Hiroshi
Iino, Takao
Ohkuma, Moriya
Sakamoto, Mitsuo
author_sort Ikeyama, Nao
collection PubMed
description A large variety of microbes are present in the human gut, some of which are considered to interact with each other. Most of these interactions involve bacterial metabolites. Phascolarctobacterium faecium hardly uses carbohydrates for growth and instead uses succinate as a substrate. This study investigated the growth behavior of the co‐culture of the succinate‐specific utilizer P. faecium and the succinogenic gut commensal Bacteroides thetaiotaomicron. Succinate production by B. thetaiotaomicron supported the growth of P. faecium and concomitant propionate production via the succinate pathway. The succinate produced was completely converted to propionate. This result was comparable with the monoculture of P. faecium in the medium supplemented with 1% (w/v) succinate. We analyzed the transcriptional response (RNA‐Seq) between the mono‐ and co‐culture of P. faecium and B. thetaiotaomicron. Comparison of the expression levels of genes of P. faecium between the mono‐ and co‐cultured conditions highlighted that the genes putatively involved in the transportation of succinate were notably expressed under the co‐cultured conditions. Differential expression analysis showed that the presence of P. faecium induced changes in the B. thetaiotaomicron transcriptional pattern, for example, expression changes in the genes for vitamin B(12) transporters and reduced expression of glutamate‐dependent acid resistance system‐related genes. Also, transcriptome analysis of P. faecium suggested that glutamate and succinate might be used as sources of succinyl‐CoA, an intermediate in the succinate pathway. This study revealed some survival strategies of asaccharolytic bacteria, such as Phascolarctobacterium spp., in the human gut.
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spelling pubmed-75682572020-10-21 Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron Ikeyama, Nao Murakami, Takumi Toyoda, Atsushi Mori, Hiroshi Iino, Takao Ohkuma, Moriya Sakamoto, Mitsuo Microbiologyopen Original Articles A large variety of microbes are present in the human gut, some of which are considered to interact with each other. Most of these interactions involve bacterial metabolites. Phascolarctobacterium faecium hardly uses carbohydrates for growth and instead uses succinate as a substrate. This study investigated the growth behavior of the co‐culture of the succinate‐specific utilizer P. faecium and the succinogenic gut commensal Bacteroides thetaiotaomicron. Succinate production by B. thetaiotaomicron supported the growth of P. faecium and concomitant propionate production via the succinate pathway. The succinate produced was completely converted to propionate. This result was comparable with the monoculture of P. faecium in the medium supplemented with 1% (w/v) succinate. We analyzed the transcriptional response (RNA‐Seq) between the mono‐ and co‐culture of P. faecium and B. thetaiotaomicron. Comparison of the expression levels of genes of P. faecium between the mono‐ and co‐cultured conditions highlighted that the genes putatively involved in the transportation of succinate were notably expressed under the co‐cultured conditions. Differential expression analysis showed that the presence of P. faecium induced changes in the B. thetaiotaomicron transcriptional pattern, for example, expression changes in the genes for vitamin B(12) transporters and reduced expression of glutamate‐dependent acid resistance system‐related genes. Also, transcriptome analysis of P. faecium suggested that glutamate and succinate might be used as sources of succinyl‐CoA, an intermediate in the succinate pathway. This study revealed some survival strategies of asaccharolytic bacteria, such as Phascolarctobacterium spp., in the human gut. John Wiley and Sons Inc. 2020-08-28 /pmc/articles/PMC7568257/ /pubmed/32856395 http://dx.doi.org/10.1002/mbo3.1111 Text en © 2020 The Authors. MicrobiologyOpen published by 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 Original Articles
Ikeyama, Nao
Murakami, Takumi
Toyoda, Atsushi
Mori, Hiroshi
Iino, Takao
Ohkuma, Moriya
Sakamoto, Mitsuo
Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron
title Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron
title_full Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron
title_fullStr Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron
title_full_unstemmed Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron
title_short Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron
title_sort microbial interaction between the succinate‐utilizing bacterium phascolarctobacterium faecium and the gut commensal bacteroides thetaiotaomicron
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7568257/
https://www.ncbi.nlm.nih.gov/pubmed/32856395
http://dx.doi.org/10.1002/mbo3.1111
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