Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron
Abstract 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 st...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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Wiley
2020-10-01
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| Series: | MicrobiologyOpen |
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| Online Access: | https://doi.org/10.1002/mbo3.1111 |
| _version_ | 1818081260606586880 |
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| author | Nao Ikeyama Takumi Murakami Atsushi Toyoda Hiroshi Mori Takao Iino Moriya Ohkuma Mitsuo Sakamoto |
| author_facet | Nao Ikeyama Takumi Murakami Atsushi Toyoda Hiroshi Mori Takao Iino Moriya Ohkuma Mitsuo Sakamoto |
| author_sort | Nao Ikeyama |
| collection | DOAJ |
| description | Abstract 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 B12 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. |
| first_indexed | 2024-12-10T19:03:23Z |
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| id | doaj.art-8f733dc55dc44cae8b907a62ca0c310a |
| institution | Directory Open Access Journal |
| issn | 2045-8827 |
| language | English |
| last_indexed | 2024-12-10T19:03:23Z |
| publishDate | 2020-10-01 |
| publisher | Wiley |
| record_format | Article |
| series | MicrobiologyOpen |
| spelling | doaj.art-8f733dc55dc44cae8b907a62ca0c310a2022-12-22T01:36:57ZengWileyMicrobiologyOpen2045-88272020-10-01910n/an/a10.1002/mbo3.1111Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicronNao Ikeyama0Takumi Murakami1Atsushi Toyoda2Hiroshi Mori3Takao Iino4Moriya Ohkuma5Mitsuo Sakamoto6Microbe Division/Japan Collection of Microorganisms RIKEN BioResource Research Center Tsukuba Ibaraki JapanAdvanced Genomics Center National Institute of Genetics Mishima Shizuoka JapanAdvanced Genomics Center National Institute of Genetics Mishima Shizuoka JapanAdvanced Genomics Center National Institute of Genetics Mishima Shizuoka JapanMicrobe Division/Japan Collection of Microorganisms RIKEN BioResource Research Center Tsukuba Ibaraki JapanMicrobe Division/Japan Collection of Microorganisms RIKEN BioResource Research Center Tsukuba Ibaraki JapanMicrobe Division/Japan Collection of Microorganisms RIKEN BioResource Research Center Tsukuba Ibaraki JapanAbstract 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 B12 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.https://doi.org/10.1002/mbo3.1111Bacteroides thetaiotaomicronPhascolarctobacterium faeciumRNA‐Seqsuccinate pathwaysurvival strategy |
| spellingShingle | Nao Ikeyama Takumi Murakami Atsushi Toyoda Hiroshi Mori Takao Iino Moriya Ohkuma Mitsuo Sakamoto Microbial interaction between the succinate‐utilizing bacterium Phascolarctobacterium faecium and the gut commensal Bacteroides thetaiotaomicron MicrobiologyOpen Bacteroides thetaiotaomicron Phascolarctobacterium faecium RNA‐Seq succinate pathway survival strategy |
| 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 | Bacteroides thetaiotaomicron Phascolarctobacterium faecium RNA‐Seq succinate pathway survival strategy |
| url | https://doi.org/10.1002/mbo3.1111 |
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