Two microbiota subtypes identified in irritable bowel syndrome with distinct responses to the low FODMAP diet
ObjectiveReducing FODMAPs (fermentable oligosaccharides, disaccharides, monosaccharides and polyols) can be clinically beneficial in IBS but the mechanism is incompletely understood. We aimed to detect microbial signatures that might predict response to the low FODMAP diet and assess whether microbi...
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| Veröffentlicht in: | Gut 2022-09, Vol.71 (9), p.1821-1830 |
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| creator | Vervier, Kevin Moss, Stephen Kumar, Nitin Adoum, Anne Barne, Meg Browne, Hilary Kaser, Arthur Kiely, Christopher J Neville, B Anne Powell, Nina Raine, Tim Stares, Mark D Zhu, Ana De La Revilla Negro, Juan Lawley, Trevor D Parkes, Miles |
| description | ObjectiveReducing FODMAPs (fermentable oligosaccharides, disaccharides, monosaccharides and polyols) can be clinically beneficial in IBS but the mechanism is incompletely understood. We aimed to detect microbial signatures that might predict response to the low FODMAP diet and assess whether microbiota compositional and functional shifts could provide insights into its mode of action.DesignWe used metagenomics to determine high-resolution taxonomic and functional profiles of the stool microbiota from IBS cases and household controls (n=56 pairs) on their usual diet. Clinical response and microbiota changes were studied in 41 pairs after 4 weeks on a low FODMAP diet.ResultsUnsupervised analysis of baseline IBS cases pre-diet identified two distinct microbiota profiles, which we refer to as IBSP (pathogenic-like) and IBSH (health-like) subtypes. IBSP microbiomes were enriched in Firmicutes and genes for amino acid and carbohydrate metabolism, but depleted in Bacteroidetes species. IBSH microbiomes were similar to controls. On the low FODMAP diet, IBSH and control microbiota were unaffected, but the IBSP signature shifted towards a health-associated microbiome with an increase in Bacteroidetes (p=0.009), a decrease in Firmicutes species (p=0.004) and normalisation of primary metabolic genes. The clinical response to the low FODMAP diet was greater in IBSP subjects compared with IBSH (p=0.02).Conclusion50% of IBS cases manifested a ‘pathogenic’ gut microbial signature. This shifted towards the healthy profile on the low FODMAP diet; and IBSP cases showed an enhanced clinical responsiveness to the dietary therapy. The effectiveness of FODMAP reduction in IBSP may result from the alterations in gut microbiota and metabolites produced. Microbiota signatures could be useful as biomarkers to guide IBS treatment; and investigating IBSP species and metabolic pathways might yield insights regarding IBS pathogenic mechanisms. |
| doi_str_mv | 10.1136/gutjnl-2021-325177 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9380505</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2601487923</sourcerecordid><originalsourceid>FETCH-LOGICAL-b469t-16c0559d3326b54c01dd20ba5ae777688019c64e376cdf1a6a49b17e897a16543</originalsourceid><addsrcrecordid>eNp9kTtvFDEUhS1ERJbAH6BAlmjSTOL3o0GKAgGkoFCE2rLH3qxXM-PF9rDafx9HE8KjoLKu_J1zfXwAeIPRGcZUnN_NdTsNHUEEd5RwLOUzsMJMqDYp9RysEMKy45LpY_CylC1CSCmNX4BjyhRGhLIVGG_3CY6xz8nFVC0ss6uHXSgw-jDVuI7BwzjBmHOs1g0BurQPAyyHyec0BriPdQN9LDVOfYU5lF2aSpPXBOsmwCHt4dXNh68X3xoU6itwtLZDCa8fzxPw_erj7eXn7vrm05fLi-vOMaFrh0WPONeeUiIcZz3C3hPkLLdBSimUQlj3ggUqRe_X2ArLtMMyKC0tFpzRE_B-8d3Nbgy-b1GyHcwux9Hmg0k2mr9vprgxd-mn0VQhjngzOH00yOnHHEo1Yyx9GAY7hTQXQwTCTElNaEPf_YNu05ynFs8QiahmiCnVKLJQ7adLyWH99BiMzEObZmnTPLRpljab6O2fMZ4kv-prwNkCuHH7e-1_HO8BePSsjQ</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2703940488</pqid></control><display><type>article</type><title>Two microbiota subtypes identified in irritable bowel syndrome with distinct responses to the low FODMAP diet</title><source>MEDLINE</source><source>PubMed Central</source><creator>Vervier, Kevin ; Moss, Stephen ; Kumar, Nitin ; Adoum, Anne ; Barne, Meg ; Browne, Hilary ; Kaser, Arthur ; Kiely, Christopher J ; Neville, B Anne ; Powell, Nina ; Raine, Tim ; Stares, Mark D ; Zhu, Ana ; De La Revilla Negro, Juan ; Lawley, Trevor D ; Parkes, Miles</creator><creatorcontrib>Vervier, Kevin ; Moss, Stephen ; Kumar, Nitin ; Adoum, Anne ; Barne, Meg ; Browne, Hilary ; Kaser, Arthur ; Kiely, Christopher J ; Neville, B Anne ; Powell, Nina ; Raine, Tim ; Stares, Mark D ; Zhu, Ana ; De La Revilla Negro, Juan ; Lawley, Trevor D ; Parkes, Miles</creatorcontrib><description>ObjectiveReducing FODMAPs (fermentable oligosaccharides, disaccharides, monosaccharides and polyols) can be clinically beneficial in IBS but the mechanism is incompletely understood. We aimed to detect microbial signatures that might predict response to the low FODMAP diet and assess whether microbiota compositional and functional shifts could provide insights into its mode of action.DesignWe used metagenomics to determine high-resolution taxonomic and functional profiles of the stool microbiota from IBS cases and household controls (n=56 pairs) on their usual diet. Clinical response and microbiota changes were studied in 41 pairs after 4 weeks on a low FODMAP diet.ResultsUnsupervised analysis of baseline IBS cases pre-diet identified two distinct microbiota profiles, which we refer to as IBSP (pathogenic-like) and IBSH (health-like) subtypes. IBSP microbiomes were enriched in Firmicutes and genes for amino acid and carbohydrate metabolism, but depleted in Bacteroidetes species. IBSH microbiomes were similar to controls. On the low FODMAP diet, IBSH and control microbiota were unaffected, but the IBSP signature shifted towards a health-associated microbiome with an increase in Bacteroidetes (p=0.009), a decrease in Firmicutes species (p=0.004) and normalisation of primary metabolic genes. The clinical response to the low FODMAP diet was greater in IBSP subjects compared with IBSH (p=0.02).Conclusion50% of IBS cases manifested a ‘pathogenic’ gut microbial signature. This shifted towards the healthy profile on the low FODMAP diet; and IBSP cases showed an enhanced clinical responsiveness to the dietary therapy. The effectiveness of FODMAP reduction in IBSP may result from the alterations in gut microbiota and metabolites produced. Microbiota signatures could be useful as biomarkers to guide IBS treatment; and investigating IBSP species and metabolic pathways might yield insights regarding IBS pathogenic mechanisms.</description><identifier>ISSN: 0017-5749</identifier><identifier>ISSN: 1468-3288</identifier><identifier>EISSN: 1468-3288</identifier><identifier>DOI: 10.1136/gutjnl-2021-325177</identifier><identifier>PMID: 34810234</identifier><language>eng</language><publisher>England: BMJ Publishing Group Ltd and British Society of Gastroenterology</publisher><subject>Alcohol use ; Amino acids ; Bacteroidetes ; Biomarkers ; Carbohydrate metabolism ; Clustering ; Diet ; Diet, Carbohydrate-Restricted ; Disaccharides ; Disaccharides - metabolism ; Fermentation ; Firmicutes ; Gastrointestinal Microbiome ; Genomes ; Households ; Humans ; intestinal microbiology ; Intestinal microflora ; Irritable Bowel Syndrome ; Metabolic pathways ; Metabolism ; Metabolites ; Metagenomics ; Microbiomes ; Microbiota ; Monosaccharides ; Nutrient deficiency ; Oligosaccharides ; Polyols ; Probiotics ; Species ; Taxonomy</subject><ispartof>Gut, 2022-09, Vol.71 (9), p.1821-1830</ispartof><rights>Author(s) (or their employer(s)) 2022. Re-use permitted under CC BY. Published by BMJ.</rights><rights>2022 Author(s) (or their employer(s)) 2022. Re-use permitted under CC BY. Published by BMJ. https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed in accordance with the Creative Commons Attribution 4.0 Unported (CC BY 4.0) license, which permits others to copy, redistribute, remix, transform and build upon this work for any purpose, provided the original work is properly cited, a link to the licence is given, and indication of whether changes were made. See: https://creativecommons.org/licenses/by/4.0/ . Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Author(s) (or their employer(s)) 2022. Re-use permitted under CC BY. Published by BMJ. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-b469t-16c0559d3326b54c01dd20ba5ae777688019c64e376cdf1a6a49b17e897a16543</citedby><cites>FETCH-LOGICAL-b469t-16c0559d3326b54c01dd20ba5ae777688019c64e376cdf1a6a49b17e897a16543</cites><orcidid>0000-0002-8497-4907 ; 0000-0002-5855-9873 ; 0000-0002-6467-0631</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9380505/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9380505/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34810234$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Vervier, Kevin</creatorcontrib><creatorcontrib>Moss, Stephen</creatorcontrib><creatorcontrib>Kumar, Nitin</creatorcontrib><creatorcontrib>Adoum, Anne</creatorcontrib><creatorcontrib>Barne, Meg</creatorcontrib><creatorcontrib>Browne, Hilary</creatorcontrib><creatorcontrib>Kaser, Arthur</creatorcontrib><creatorcontrib>Kiely, Christopher J</creatorcontrib><creatorcontrib>Neville, B Anne</creatorcontrib><creatorcontrib>Powell, Nina</creatorcontrib><creatorcontrib>Raine, Tim</creatorcontrib><creatorcontrib>Stares, Mark D</creatorcontrib><creatorcontrib>Zhu, Ana</creatorcontrib><creatorcontrib>De La Revilla Negro, Juan</creatorcontrib><creatorcontrib>Lawley, Trevor D</creatorcontrib><creatorcontrib>Parkes, Miles</creatorcontrib><title>Two microbiota subtypes identified in irritable bowel syndrome with distinct responses to the low FODMAP diet</title><title>Gut</title><addtitle>Gut</addtitle><addtitle>Gut</addtitle><description>ObjectiveReducing FODMAPs (fermentable oligosaccharides, disaccharides, monosaccharides and polyols) can be clinically beneficial in IBS but the mechanism is incompletely understood. We aimed to detect microbial signatures that might predict response to the low FODMAP diet and assess whether microbiota compositional and functional shifts could provide insights into its mode of action.DesignWe used metagenomics to determine high-resolution taxonomic and functional profiles of the stool microbiota from IBS cases and household controls (n=56 pairs) on their usual diet. Clinical response and microbiota changes were studied in 41 pairs after 4 weeks on a low FODMAP diet.ResultsUnsupervised analysis of baseline IBS cases pre-diet identified two distinct microbiota profiles, which we refer to as IBSP (pathogenic-like) and IBSH (health-like) subtypes. IBSP microbiomes were enriched in Firmicutes and genes for amino acid and carbohydrate metabolism, but depleted in Bacteroidetes species. IBSH microbiomes were similar to controls. On the low FODMAP diet, IBSH and control microbiota were unaffected, but the IBSP signature shifted towards a health-associated microbiome with an increase in Bacteroidetes (p=0.009), a decrease in Firmicutes species (p=0.004) and normalisation of primary metabolic genes. The clinical response to the low FODMAP diet was greater in IBSP subjects compared with IBSH (p=0.02).Conclusion50% of IBS cases manifested a ‘pathogenic’ gut microbial signature. This shifted towards the healthy profile on the low FODMAP diet; and IBSP cases showed an enhanced clinical responsiveness to the dietary therapy. The effectiveness of FODMAP reduction in IBSP may result from the alterations in gut microbiota and metabolites produced. Microbiota signatures could be useful as biomarkers to guide IBS treatment; and investigating IBSP species and metabolic pathways might yield insights regarding IBS pathogenic mechanisms.</description><subject>Alcohol use</subject><subject>Amino acids</subject><subject>Bacteroidetes</subject><subject>Biomarkers</subject><subject>Carbohydrate metabolism</subject><subject>Clustering</subject><subject>Diet</subject><subject>Diet, Carbohydrate-Restricted</subject><subject>Disaccharides</subject><subject>Disaccharides - metabolism</subject><subject>Fermentation</subject><subject>Firmicutes</subject><subject>Gastrointestinal Microbiome</subject><subject>Genomes</subject><subject>Households</subject><subject>Humans</subject><subject>intestinal microbiology</subject><subject>Intestinal microflora</subject><subject>Irritable Bowel Syndrome</subject><subject>Metabolic pathways</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Metagenomics</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Monosaccharides</subject><subject>Nutrient deficiency</subject><subject>Oligosaccharides</subject><subject>Polyols</subject><subject>Probiotics</subject><subject>Species</subject><subject>Taxonomy</subject><issn>0017-5749</issn><issn>1468-3288</issn><issn>1468-3288</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>9YT</sourceid><sourceid>ACMMV</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kTtvFDEUhS1ERJbAH6BAlmjSTOL3o0GKAgGkoFCE2rLH3qxXM-PF9rDafx9HE8KjoLKu_J1zfXwAeIPRGcZUnN_NdTsNHUEEd5RwLOUzsMJMqDYp9RysEMKy45LpY_CylC1CSCmNX4BjyhRGhLIVGG_3CY6xz8nFVC0ss6uHXSgw-jDVuI7BwzjBmHOs1g0BurQPAyyHyec0BriPdQN9LDVOfYU5lF2aSpPXBOsmwCHt4dXNh68X3xoU6itwtLZDCa8fzxPw_erj7eXn7vrm05fLi-vOMaFrh0WPONeeUiIcZz3C3hPkLLdBSimUQlj3ggUqRe_X2ArLtMMyKC0tFpzRE_B-8d3Nbgy-b1GyHcwux9Hmg0k2mr9vprgxd-mn0VQhjngzOH00yOnHHEo1Yyx9GAY7hTQXQwTCTElNaEPf_YNu05ynFs8QiahmiCnVKLJQ7adLyWH99BiMzEObZmnTPLRpljab6O2fMZ4kv-prwNkCuHH7e-1_HO8BePSsjQ</recordid><startdate>202209</startdate><enddate>202209</enddate><creator>Vervier, 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microbiota subtypes identified in irritable bowel syndrome with distinct responses to the low FODMAP diet</title><author>Vervier, Kevin ; Moss, Stephen ; Kumar, Nitin ; Adoum, Anne ; Barne, Meg ; Browne, Hilary ; Kaser, Arthur ; Kiely, Christopher J ; Neville, B Anne ; Powell, Nina ; Raine, Tim ; Stares, Mark D ; Zhu, Ana ; De La Revilla Negro, Juan ; Lawley, Trevor D ; Parkes, Miles</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-b469t-16c0559d3326b54c01dd20ba5ae777688019c64e376cdf1a6a49b17e897a16543</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Alcohol use</topic><topic>Amino acids</topic><topic>Bacteroidetes</topic><topic>Biomarkers</topic><topic>Carbohydrate metabolism</topic><topic>Clustering</topic><topic>Diet</topic><topic>Diet, Carbohydrate-Restricted</topic><topic>Disaccharides</topic><topic>Disaccharides - metabolism</topic><topic>Fermentation</topic><topic>Firmicutes</topic><topic>Gastrointestinal Microbiome</topic><topic>Genomes</topic><topic>Households</topic><topic>Humans</topic><topic>intestinal microbiology</topic><topic>Intestinal microflora</topic><topic>Irritable Bowel Syndrome</topic><topic>Metabolic pathways</topic><topic>Metabolism</topic><topic>Metabolites</topic><topic>Metagenomics</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Monosaccharides</topic><topic>Nutrient deficiency</topic><topic>Oligosaccharides</topic><topic>Polyols</topic><topic>Probiotics</topic><topic>Species</topic><topic>Taxonomy</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Vervier, Kevin</creatorcontrib><creatorcontrib>Moss, Stephen</creatorcontrib><creatorcontrib>Kumar, Nitin</creatorcontrib><creatorcontrib>Adoum, Anne</creatorcontrib><creatorcontrib>Barne, Meg</creatorcontrib><creatorcontrib>Browne, Hilary</creatorcontrib><creatorcontrib>Kaser, Arthur</creatorcontrib><creatorcontrib>Kiely, Christopher J</creatorcontrib><creatorcontrib>Neville, B Anne</creatorcontrib><creatorcontrib>Powell, Nina</creatorcontrib><creatorcontrib>Raine, Tim</creatorcontrib><creatorcontrib>Stares, Mark D</creatorcontrib><creatorcontrib>Zhu, Ana</creatorcontrib><creatorcontrib>De La Revilla Negro, Juan</creatorcontrib><creatorcontrib>Lawley, Trevor D</creatorcontrib><creatorcontrib>Parkes, Miles</creatorcontrib><collection>BMJ Open Access Journals</collection><collection>BMJ Journals:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 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Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Vervier, Kevin</au><au>Moss, Stephen</au><au>Kumar, Nitin</au><au>Adoum, Anne</au><au>Barne, Meg</au><au>Browne, Hilary</au><au>Kaser, Arthur</au><au>Kiely, Christopher J</au><au>Neville, B Anne</au><au>Powell, Nina</au><au>Raine, Tim</au><au>Stares, Mark D</au><au>Zhu, Ana</au><au>De La Revilla Negro, Juan</au><au>Lawley, Trevor D</au><au>Parkes, Miles</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Two microbiota subtypes identified in irritable bowel syndrome with distinct responses to the low FODMAP diet</atitle><jtitle>Gut</jtitle><stitle>Gut</stitle><addtitle>Gut</addtitle><date>2022-09</date><risdate>2022</risdate><volume>71</volume><issue>9</issue><spage>1821</spage><epage>1830</epage><pages>1821-1830</pages><issn>0017-5749</issn><issn>1468-3288</issn><eissn>1468-3288</eissn><abstract>ObjectiveReducing FODMAPs (fermentable oligosaccharides, disaccharides, monosaccharides and polyols) can be clinically beneficial in IBS but the mechanism is incompletely understood. We aimed to detect microbial signatures that might predict response to the low FODMAP diet and assess whether microbiota compositional and functional shifts could provide insights into its mode of action.DesignWe used metagenomics to determine high-resolution taxonomic and functional profiles of the stool microbiota from IBS cases and household controls (n=56 pairs) on their usual diet. Clinical response and microbiota changes were studied in 41 pairs after 4 weeks on a low FODMAP diet.ResultsUnsupervised analysis of baseline IBS cases pre-diet identified two distinct microbiota profiles, which we refer to as IBSP (pathogenic-like) and IBSH (health-like) subtypes. IBSP microbiomes were enriched in Firmicutes and genes for amino acid and carbohydrate metabolism, but depleted in Bacteroidetes species. IBSH microbiomes were similar to controls. On the low FODMAP diet, IBSH and control microbiota were unaffected, but the IBSP signature shifted towards a health-associated microbiome with an increase in Bacteroidetes (p=0.009), a decrease in Firmicutes species (p=0.004) and normalisation of primary metabolic genes. The clinical response to the low FODMAP diet was greater in IBSP subjects compared with IBSH (p=0.02).Conclusion50% of IBS cases manifested a ‘pathogenic’ gut microbial signature. This shifted towards the healthy profile on the low FODMAP diet; and IBSP cases showed an enhanced clinical responsiveness to the dietary therapy. The effectiveness of FODMAP reduction in IBSP may result from the alterations in gut microbiota and metabolites produced. Microbiota signatures could be useful as biomarkers to guide IBS treatment; and investigating IBSP species and metabolic pathways might yield insights regarding IBS pathogenic mechanisms.</abstract><cop>England</cop><pub>BMJ Publishing Group Ltd and British Society of Gastroenterology</pub><pmid>34810234</pmid><doi>10.1136/gutjnl-2021-325177</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-8497-4907</orcidid><orcidid>https://orcid.org/0000-0002-5855-9873</orcidid><orcidid>https://orcid.org/0000-0002-6467-0631</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Alcohol use Amino acids Bacteroidetes Biomarkers Carbohydrate metabolism Clustering Diet Diet, Carbohydrate-Restricted Disaccharides Disaccharides - metabolism Fermentation Firmicutes Gastrointestinal Microbiome Genomes Households Humans intestinal microbiology Intestinal microflora Irritable Bowel Syndrome Metabolic pathways Metabolism Metabolites Metagenomics Microbiomes Microbiota Monosaccharides Nutrient deficiency Oligosaccharides Polyols Probiotics Species Taxonomy |
| title | Two microbiota subtypes identified in irritable bowel syndrome with distinct responses to the low FODMAP diet |
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