Dietary- and host-derived metabolites are used by diverse gut bacteria for anaerobic respiration
Respiratory reductases enable microorganisms to use molecules present in anaerobic ecosystems as energy-generating respiratory electron acceptors. Here we identify three taxonomically distinct families of human gut bacteria (Burkholderiaceae, Eggerthellaceae and Erysipelotrichaceae) that encode larg...
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Veröffentlicht in: | Nature microbiology 2024-01, Vol.9 (1), p.55-69 |
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creator | Little, Alexander S. Younker, Isaac T. Schechter, Matthew S. Bernardino, Paola Nol Méheust, Raphaël Stemczynski, Joshua Scorza, Kaylie Mullowney, Michael W. Sharan, Deepti Waligurski, Emily Smith, Rita Ramanswamy, Ramanujam Leiter, William Moran, David McMillin, Mary Odenwald, Matthew A. Iavarone, Anthony T. Sidebottom, Ashley M. Sundararajan, Anitha Pamer, Eric G. Eren, A. Murat Light, Samuel H. |
description | Respiratory reductases enable microorganisms to use molecules present in anaerobic ecosystems as energy-generating respiratory electron acceptors. Here we identify three taxonomically distinct families of human gut bacteria (Burkholderiaceae, Eggerthellaceae and Erysipelotrichaceae) that encode large arsenals of tens to hundreds of respiratory-like reductases per genome. Screening species from each family (
Sutterella wadsworthensis
,
Eggerthella lenta
and
Holdemania filiformis
), we discover 22 metabolites used as respiratory electron acceptors in a species-specific manner. Identified reactions transform multiple classes of dietary- and host-derived metabolites, including bioactive molecules resveratrol and itaconate. Products of identified respiratory metabolisms highlight poorly characterized compounds, such as the itaconate-derived 2-methylsuccinate. Reductase substrate profiling defines enzyme–substrate pairs and reveals a complex picture of reductase evolution, providing evidence that reductases with specificities for related cinnamate substrates independently emerged at least four times. These studies thus establish an exceptionally versatile form of anaerobic respiration that directly links microbial energy metabolism to the gut metabolome.
Three distinct families of gut bacteria encode an unprecedented number of respiratory-like reductases per genome to perform anaerobic respiration of biomedically relevant substrates. |
doi_str_mv | 10.1038/s41564-023-01560-2 |
format | Article |
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Sutterella wadsworthensis
,
Eggerthella lenta
and
Holdemania filiformis
), we discover 22 metabolites used as respiratory electron acceptors in a species-specific manner. Identified reactions transform multiple classes of dietary- and host-derived metabolites, including bioactive molecules resveratrol and itaconate. Products of identified respiratory metabolisms highlight poorly characterized compounds, such as the itaconate-derived 2-methylsuccinate. Reductase substrate profiling defines enzyme–substrate pairs and reveals a complex picture of reductase evolution, providing evidence that reductases with specificities for related cinnamate substrates independently emerged at least four times. These studies thus establish an exceptionally versatile form of anaerobic respiration that directly links microbial energy metabolism to the gut metabolome.
Three distinct families of gut bacteria encode an unprecedented number of respiratory-like reductases per genome to perform anaerobic respiration of biomedically relevant substrates.</description><identifier>ISSN: 2058-5276</identifier><identifier>EISSN: 2058-5276</identifier><identifier>DOI: 10.1038/s41564-023-01560-2</identifier><identifier>PMID: 38177297</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/39 ; 45/43 ; 631/326/1320 ; 631/326/2565/2134 ; 631/45/320 ; 631/45/607/1168 ; 64/60 ; 82/58 ; 82/80 ; Anaerobic microorganisms ; Anaerobic respiration ; Anaerobiosis ; Bacteria ; Bacteria - genetics ; Bacteria - metabolism ; Biomedical and Life Sciences ; Ecosystem ; Energy metabolism ; Genomes ; Humans ; Infectious Diseases ; Life Sciences ; Medical Microbiology ; Metabolites ; Microbiology ; Oxidoreductases - genetics ; Oxidoreductases - metabolism ; Parasitology ; Respiration ; Resveratrol ; Virology</subject><ispartof>Nature microbiology, 2024-01, Vol.9 (1), p.55-69</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2024. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2024. The Author(s), under exclusive licence to Springer Nature Limited.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c475t-1db9d497bcc63b944060943dd648eeea5c55b8f05f523480f5e4c562938c03db3</citedby><cites>FETCH-LOGICAL-c475t-1db9d497bcc63b944060943dd648eeea5c55b8f05f523480f5e4c562938c03db3</cites><orcidid>0000-0003-2365-8828 ; 0000-0003-1740-6472 ; 0000-0002-2556-1707 ; 0000-0002-8435-3203 ; 0000-0002-4847-426X ; 0000-0002-7022-9068 ; 0000-0002-8074-1348 ; 0000-0002-6755-9904 ; 0000-0001-7448-6574 ; 0000-0002-2884-4307 ; 0000-0001-9013-4827 ; 0000-0002-7546-5019 ; 0000-0002-8327-1935</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,781,785,886,27929,27930</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38177297$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Little, Alexander S.</creatorcontrib><creatorcontrib>Younker, Isaac T.</creatorcontrib><creatorcontrib>Schechter, Matthew S.</creatorcontrib><creatorcontrib>Bernardino, Paola Nol</creatorcontrib><creatorcontrib>Méheust, Raphaël</creatorcontrib><creatorcontrib>Stemczynski, Joshua</creatorcontrib><creatorcontrib>Scorza, Kaylie</creatorcontrib><creatorcontrib>Mullowney, Michael W.</creatorcontrib><creatorcontrib>Sharan, Deepti</creatorcontrib><creatorcontrib>Waligurski, Emily</creatorcontrib><creatorcontrib>Smith, Rita</creatorcontrib><creatorcontrib>Ramanswamy, Ramanujam</creatorcontrib><creatorcontrib>Leiter, William</creatorcontrib><creatorcontrib>Moran, David</creatorcontrib><creatorcontrib>McMillin, Mary</creatorcontrib><creatorcontrib>Odenwald, Matthew A.</creatorcontrib><creatorcontrib>Iavarone, Anthony T.</creatorcontrib><creatorcontrib>Sidebottom, Ashley M.</creatorcontrib><creatorcontrib>Sundararajan, Anitha</creatorcontrib><creatorcontrib>Pamer, Eric G.</creatorcontrib><creatorcontrib>Eren, A. Murat</creatorcontrib><creatorcontrib>Light, Samuel H.</creatorcontrib><title>Dietary- and host-derived metabolites are used by diverse gut bacteria for anaerobic respiration</title><title>Nature microbiology</title><addtitle>Nat Microbiol</addtitle><addtitle>Nat Microbiol</addtitle><description>Respiratory reductases enable microorganisms to use molecules present in anaerobic ecosystems as energy-generating respiratory electron acceptors. Here we identify three taxonomically distinct families of human gut bacteria (Burkholderiaceae, Eggerthellaceae and Erysipelotrichaceae) that encode large arsenals of tens to hundreds of respiratory-like reductases per genome. Screening species from each family (
Sutterella wadsworthensis
,
Eggerthella lenta
and
Holdemania filiformis
), we discover 22 metabolites used as respiratory electron acceptors in a species-specific manner. Identified reactions transform multiple classes of dietary- and host-derived metabolites, including bioactive molecules resveratrol and itaconate. Products of identified respiratory metabolisms highlight poorly characterized compounds, such as the itaconate-derived 2-methylsuccinate. Reductase substrate profiling defines enzyme–substrate pairs and reveals a complex picture of reductase evolution, providing evidence that reductases with specificities for related cinnamate substrates independently emerged at least four times. These studies thus establish an exceptionally versatile form of anaerobic respiration that directly links microbial energy metabolism to the gut metabolome.
Three distinct families of gut bacteria encode an unprecedented number of respiratory-like reductases per genome to perform anaerobic respiration of biomedically relevant substrates.</description><subject>38/39</subject><subject>45/43</subject><subject>631/326/1320</subject><subject>631/326/2565/2134</subject><subject>631/45/320</subject><subject>631/45/607/1168</subject><subject>64/60</subject><subject>82/58</subject><subject>82/80</subject><subject>Anaerobic microorganisms</subject><subject>Anaerobic respiration</subject><subject>Anaerobiosis</subject><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Bacteria - metabolism</subject><subject>Biomedical and Life Sciences</subject><subject>Ecosystem</subject><subject>Energy metabolism</subject><subject>Genomes</subject><subject>Humans</subject><subject>Infectious Diseases</subject><subject>Life Sciences</subject><subject>Medical Microbiology</subject><subject>Metabolites</subject><subject>Microbiology</subject><subject>Oxidoreductases - genetics</subject><subject>Oxidoreductases - metabolism</subject><subject>Parasitology</subject><subject>Respiration</subject><subject>Resveratrol</subject><subject>Virology</subject><issn>2058-5276</issn><issn>2058-5276</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU1PFTEYhRujEYL8ARemiRs3xX5PZ2UMqJiQuIF17cc7l5K502vbIeHfW7yI6MJV3_Q872lPDkKvGT1hVJj3VTKlJaFcENonSvgzdMipMkTxQT9_Mh-g41pvKKVMc62NfokOhGHDwMfhEH0_S9BcuSPYLRFf59pIhJJuIeJtF3yeU4OKXQG81n7p73DsaqmAN2vD3oXWcYenXLqDg5J9CrhA3aXiWsrLK_RicnOF44fzCF19_nR5ek4uvn35evrxggQ5qEZY9GOU4-BD0MKPUlJNRyli1NIAgFNBKW8mqibFhTR0UiCD0nwUJlARvThCH_a-u9VvIQZYWnGz3ZW07fFsdsn-rSzp2m7yrWWMKiWV6A7vHhxK_rFCbXabaoB5dgvktVo-MmYkF9x09O0_6E1ey9Lz3VN0EIIL1Sm-p0LJtRaYHn_DqL0v0e5LtL1E-6tEy_vSm6c5Hld-V9YBsQdql5YNlD9v_8f2J0lGqD8</recordid><startdate>20240101</startdate><enddate>20240101</enddate><creator>Little, Alexander S.</creator><creator>Younker, Isaac T.</creator><creator>Schechter, Matthew S.</creator><creator>Bernardino, Paola Nol</creator><creator>Méheust, Raphaël</creator><creator>Stemczynski, Joshua</creator><creator>Scorza, Kaylie</creator><creator>Mullowney, Michael W.</creator><creator>Sharan, Deepti</creator><creator>Waligurski, Emily</creator><creator>Smith, Rita</creator><creator>Ramanswamy, Ramanujam</creator><creator>Leiter, William</creator><creator>Moran, David</creator><creator>McMillin, Mary</creator><creator>Odenwald, Matthew A.</creator><creator>Iavarone, Anthony T.</creator><creator>Sidebottom, Ashley M.</creator><creator>Sundararajan, Anitha</creator><creator>Pamer, Eric G.</creator><creator>Eren, A. 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Murat</au><au>Light, Samuel H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dietary- and host-derived metabolites are used by diverse gut bacteria for anaerobic respiration</atitle><jtitle>Nature microbiology</jtitle><stitle>Nat Microbiol</stitle><addtitle>Nat Microbiol</addtitle><date>2024-01-01</date><risdate>2024</risdate><volume>9</volume><issue>1</issue><spage>55</spage><epage>69</epage><pages>55-69</pages><issn>2058-5276</issn><eissn>2058-5276</eissn><abstract>Respiratory reductases enable microorganisms to use molecules present in anaerobic ecosystems as energy-generating respiratory electron acceptors. Here we identify three taxonomically distinct families of human gut bacteria (Burkholderiaceae, Eggerthellaceae and Erysipelotrichaceae) that encode large arsenals of tens to hundreds of respiratory-like reductases per genome. Screening species from each family (
Sutterella wadsworthensis
,
Eggerthella lenta
and
Holdemania filiformis
), we discover 22 metabolites used as respiratory electron acceptors in a species-specific manner. Identified reactions transform multiple classes of dietary- and host-derived metabolites, including bioactive molecules resveratrol and itaconate. Products of identified respiratory metabolisms highlight poorly characterized compounds, such as the itaconate-derived 2-methylsuccinate. Reductase substrate profiling defines enzyme–substrate pairs and reveals a complex picture of reductase evolution, providing evidence that reductases with specificities for related cinnamate substrates independently emerged at least four times. These studies thus establish an exceptionally versatile form of anaerobic respiration that directly links microbial energy metabolism to the gut metabolome.
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subjects | 38/39 45/43 631/326/1320 631/326/2565/2134 631/45/320 631/45/607/1168 64/60 82/58 82/80 Anaerobic microorganisms Anaerobic respiration Anaerobiosis Bacteria Bacteria - genetics Bacteria - metabolism Biomedical and Life Sciences Ecosystem Energy metabolism Genomes Humans Infectious Diseases Life Sciences Medical Microbiology Metabolites Microbiology Oxidoreductases - genetics Oxidoreductases - metabolism Parasitology Respiration Resveratrol Virology |
title | Dietary- and host-derived metabolites are used by diverse gut bacteria for anaerobic respiration |
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