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Elevated circulating levels of succinate in human obesity are linked to specific gut microbiota
Gut microbiota-related metabolites are potential clinical biomarkers for cardiovascular disease (CVD). Circulating succinate, a metabolite produced by both microbiota and the host, is increased in hypertension, ischemic heart disease, and type 2 diabetes. We aimed to analyze systemic levels of succi...
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| Published in: | The ISME Journal 2018-07, Vol.12 (7), p.1642-1657 |
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| container_end_page | 1657 |
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| container_title | The ISME Journal |
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| creator | Serena, Carolina Ceperuelo-Mallafré, Victoria Keiran, Noelia Queipo-Ortuño, Maria Isabel Bernal, Rosa Gomez-Huelgas, Ricardo Urpi-Sarda, Mireia Sabater, Mónica Pérez-Brocal, Vicente Andrés-Lacueva, Cristina Moya, Andres Tinahones, Francisco J Fernández-Real, Jose Manuel Vendrell, Joan Fernández-Veledo, Sonia |
| description | Gut microbiota-related metabolites are potential clinical biomarkers for cardiovascular disease (CVD). Circulating succinate, a metabolite produced by both microbiota and the host, is increased in hypertension, ischemic heart disease, and type 2 diabetes. We aimed to analyze systemic levels of succinate in obesity, a major risk factor for CVD, and its relationship with gut microbiome. We explored the association of circulating succinate with specific metagenomic signatures in cross-sectional and prospective cohorts of Caucasian Spanish subjects. Obesity was associated with elevated levels of circulating succinate concomitant with impaired glucose metabolism. This increase was associated with specific changes in gut microbiota related to succinate metabolism: a higher relative abundance of succinate-producing
Prevotellaceae
(P)
and Veillonellaceae
(V), and a lower relative abundance of succinate-consuming
Odoribacteraceae
(O) and
Clostridaceae
(C) in obese individuals, with the (P + V/O + C) ratio being a main determinant of plasma succinate. Weight loss intervention decreased (P + V/O + C) ratio coincident with the reduction in circulating succinate. In the spontaneous evolution after good dietary advice, alterations in circulating succinate levels were linked to specific metagenomic signatures associated with carbohydrate metabolism and energy production with independence of body weight change. Our data support the importance of microbe–microbe interactions for the metabolite signature of gut microbiome and uncover succinate as a potential microbiota-derived metabolite related to CVD risk. |
| doi_str_mv | 10.1038/s41396-018-0068-2 |
| format | article |
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Prevotellaceae
(P)
and Veillonellaceae
(V), and a lower relative abundance of succinate-consuming
Odoribacteraceae
(O) and
Clostridaceae
(C) in obese individuals, with the (P + V/O + C) ratio being a main determinant of plasma succinate. Weight loss intervention decreased (P + V/O + C) ratio coincident with the reduction in circulating succinate. In the spontaneous evolution after good dietary advice, alterations in circulating succinate levels were linked to specific metagenomic signatures associated with carbohydrate metabolism and energy production with independence of body weight change. Our data support the importance of microbe–microbe interactions for the metabolite signature of gut microbiome and uncover succinate as a potential microbiota-derived metabolite related to CVD risk.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/s41396-018-0068-2</identifier><identifier>PMID: 29434314</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>38/22 ; 38/23 ; 38/39 ; 38/43 ; 45/77 ; 631/1647/514/2254 ; 631/326/2565/2134 ; 631/326/2565/2142 ; 692/420 ; 692/53 ; Abundance ; Adult ; Aged ; Bacteria - classification ; Bacteria - genetics ; Bacteria - isolation & purification ; Bacteria - metabolism ; Biomarkers ; Biomarkers - blood ; Biomedical and Life Sciences ; Body weight ; Body weight loss ; Carbohydrate metabolism ; Carbohydrates ; Cardiovascular diseases ; Coronary artery disease ; Cross-Sectional Studies ; Diabetes mellitus ; Diabetes mellitus (non-insulin dependent) ; Diabetes Mellitus, Type 2 - blood ; Diabetes Mellitus, Type 2 - microbiology ; Diet ; Dieta ; Ecology ; Energy metabolism ; Evolutionary Biology ; Female ; Gastrointestinal Microbiome ; Glucose metabolism ; Heart diseases ; Humans ; Hypertension ; Intestinal microflora ; Ischemia ; Life Sciences ; Male ; Metabolism ; Metabolites ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Microbiomes ; Microbiota ; Microbiota intestinal ; Middle Aged ; Obesitat ; Obesity ; Obesity - blood ; Obesity - microbiology ; Phylogeny ; Prospective Studies ; Relative abundance ; Risk factors ; Succinic Acid - blood ; Weight control</subject><ispartof>The ISME Journal, 2018-07, Vol.12 (7), p.1642-1657</ispartof><rights>The Author(s) 2018</rights><rights>2018. This work is published under http://creativecommons.org/licenses/by-nc-nd/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>cc-by (c) Serena, Carolina et al., 2018 info:eu-repo/semantics/openAccess <a href="http://creativecommons.org/licenses/by/3.0/es">http://creativecommons.org/licenses/by/3.0/es</a></rights><rights>The Author(s) 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c578t-9473427475aa4a5f215ebe09cf86652f2bcd7bbca52b7b87b72fdcaaf868d59d3</citedby><cites>FETCH-LOGICAL-c578t-9473427475aa4a5f215ebe09cf86652f2bcd7bbca52b7b87b72fdcaaf868d59d3</cites><orcidid>0000-0002-2867-1119</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/PMC6018807/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6018807/$$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/29434314$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Serena, Carolina</creatorcontrib><creatorcontrib>Ceperuelo-Mallafré, Victoria</creatorcontrib><creatorcontrib>Keiran, Noelia</creatorcontrib><creatorcontrib>Queipo-Ortuño, Maria Isabel</creatorcontrib><creatorcontrib>Bernal, Rosa</creatorcontrib><creatorcontrib>Gomez-Huelgas, Ricardo</creatorcontrib><creatorcontrib>Urpi-Sarda, Mireia</creatorcontrib><creatorcontrib>Sabater, Mónica</creatorcontrib><creatorcontrib>Pérez-Brocal, Vicente</creatorcontrib><creatorcontrib>Andrés-Lacueva, Cristina</creatorcontrib><creatorcontrib>Moya, Andres</creatorcontrib><creatorcontrib>Tinahones, Francisco J</creatorcontrib><creatorcontrib>Fernández-Real, Jose Manuel</creatorcontrib><creatorcontrib>Vendrell, Joan</creatorcontrib><creatorcontrib>Fernández-Veledo, Sonia</creatorcontrib><title>Elevated circulating levels of succinate in human obesity are linked to specific gut microbiota</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>Gut microbiota-related metabolites are potential clinical biomarkers for cardiovascular disease (CVD). Circulating succinate, a metabolite produced by both microbiota and the host, is increased in hypertension, ischemic heart disease, and type 2 diabetes. We aimed to analyze systemic levels of succinate in obesity, a major risk factor for CVD, and its relationship with gut microbiome. We explored the association of circulating succinate with specific metagenomic signatures in cross-sectional and prospective cohorts of Caucasian Spanish subjects. Obesity was associated with elevated levels of circulating succinate concomitant with impaired glucose metabolism. This increase was associated with specific changes in gut microbiota related to succinate metabolism: a higher relative abundance of succinate-producing
Prevotellaceae
(P)
and Veillonellaceae
(V), and a lower relative abundance of succinate-consuming
Odoribacteraceae
(O) and
Clostridaceae
(C) in obese individuals, with the (P + V/O + C) ratio being a main determinant of plasma succinate. Weight loss intervention decreased (P + V/O + C) ratio coincident with the reduction in circulating succinate. In the spontaneous evolution after good dietary advice, alterations in circulating succinate levels were linked to specific metagenomic signatures associated with carbohydrate metabolism and energy production with independence of body weight change. Our data support the importance of microbe–microbe interactions for the metabolite signature of gut microbiome and uncover succinate as a potential microbiota-derived metabolite related to CVD risk.</description><subject>38/22</subject><subject>38/23</subject><subject>38/39</subject><subject>38/43</subject><subject>45/77</subject><subject>631/1647/514/2254</subject><subject>631/326/2565/2134</subject><subject>631/326/2565/2142</subject><subject>692/420</subject><subject>692/53</subject><subject>Abundance</subject><subject>Adult</subject><subject>Aged</subject><subject>Bacteria - classification</subject><subject>Bacteria - genetics</subject><subject>Bacteria - isolation & purification</subject><subject>Bacteria - metabolism</subject><subject>Biomarkers</subject><subject>Biomarkers - blood</subject><subject>Biomedical and Life Sciences</subject><subject>Body weight</subject><subject>Body weight loss</subject><subject>Carbohydrate metabolism</subject><subject>Carbohydrates</subject><subject>Cardiovascular diseases</subject><subject>Coronary artery disease</subject><subject>Cross-Sectional Studies</subject><subject>Diabetes mellitus</subject><subject>Diabetes mellitus (non-insulin dependent)</subject><subject>Diabetes Mellitus, Type 2 - blood</subject><subject>Diabetes Mellitus, Type 2 - microbiology</subject><subject>Diet</subject><subject>Dieta</subject><subject>Ecology</subject><subject>Energy metabolism</subject><subject>Evolutionary Biology</subject><subject>Female</subject><subject>Gastrointestinal Microbiome</subject><subject>Glucose metabolism</subject><subject>Heart diseases</subject><subject>Humans</subject><subject>Hypertension</subject><subject>Intestinal microflora</subject><subject>Ischemia</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Metabolism</subject><subject>Metabolites</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microbiota intestinal</subject><subject>Middle Aged</subject><subject>Obesitat</subject><subject>Obesity</subject><subject>Obesity - blood</subject><subject>Obesity - microbiology</subject><subject>Phylogeny</subject><subject>Prospective Studies</subject><subject>Relative abundance</subject><subject>Risk factors</subject><subject>Succinic Acid - 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Academic</collection><collection>Recercat</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Serena, Carolina</au><au>Ceperuelo-Mallafré, Victoria</au><au>Keiran, Noelia</au><au>Queipo-Ortuño, Maria Isabel</au><au>Bernal, Rosa</au><au>Gomez-Huelgas, Ricardo</au><au>Urpi-Sarda, Mireia</au><au>Sabater, Mónica</au><au>Pérez-Brocal, Vicente</au><au>Andrés-Lacueva, Cristina</au><au>Moya, Andres</au><au>Tinahones, Francisco J</au><au>Fernández-Real, Jose Manuel</au><au>Vendrell, Joan</au><au>Fernández-Veledo, Sonia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Elevated circulating levels of succinate in human obesity are linked to specific gut microbiota</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2018-07-01</date><risdate>2018</risdate><volume>12</volume><issue>7</issue><spage>1642</spage><epage>1657</epage><pages>1642-1657</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>Gut microbiota-related metabolites are potential clinical biomarkers for cardiovascular disease (CVD). Circulating succinate, a metabolite produced by both microbiota and the host, is increased in hypertension, ischemic heart disease, and type 2 diabetes. We aimed to analyze systemic levels of succinate in obesity, a major risk factor for CVD, and its relationship with gut microbiome. We explored the association of circulating succinate with specific metagenomic signatures in cross-sectional and prospective cohorts of Caucasian Spanish subjects. Obesity was associated with elevated levels of circulating succinate concomitant with impaired glucose metabolism. This increase was associated with specific changes in gut microbiota related to succinate metabolism: a higher relative abundance of succinate-producing
Prevotellaceae
(P)
and Veillonellaceae
(V), and a lower relative abundance of succinate-consuming
Odoribacteraceae
(O) and
Clostridaceae
(C) in obese individuals, with the (P + V/O + C) ratio being a main determinant of plasma succinate. Weight loss intervention decreased (P + V/O + C) ratio coincident with the reduction in circulating succinate. In the spontaneous evolution after good dietary advice, alterations in circulating succinate levels were linked to specific metagenomic signatures associated with carbohydrate metabolism and energy production with independence of body weight change. Our data support the importance of microbe–microbe interactions for the metabolite signature of gut microbiome and uncover succinate as a potential microbiota-derived metabolite related to CVD risk.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>29434314</pmid><doi>10.1038/s41396-018-0068-2</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-2867-1119</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1751-7362 |
| ispartof | The ISME Journal, 2018-07, Vol.12 (7), p.1642-1657 |
| issn | 1751-7362 1751-7370 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6018807 |
| source | PubMed (Medline); Springer Link; Oxford Open Access Journals |
| subjects | 38/22 38/23 38/39 38/43 45/77 631/1647/514/2254 631/326/2565/2134 631/326/2565/2142 692/420 692/53 Abundance Adult Aged Bacteria - classification Bacteria - genetics Bacteria - isolation & purification Bacteria - metabolism Biomarkers Biomarkers - blood Biomedical and Life Sciences Body weight Body weight loss Carbohydrate metabolism Carbohydrates Cardiovascular diseases Coronary artery disease Cross-Sectional Studies Diabetes mellitus Diabetes mellitus (non-insulin dependent) Diabetes Mellitus, Type 2 - blood Diabetes Mellitus, Type 2 - microbiology Diet Dieta Ecology Energy metabolism Evolutionary Biology Female Gastrointestinal Microbiome Glucose metabolism Heart diseases Humans Hypertension Intestinal microflora Ischemia Life Sciences Male Metabolism Metabolites Microbial Ecology Microbial Genetics and Genomics Microbiology Microbiomes Microbiota Microbiota intestinal Middle Aged Obesitat Obesity Obesity - blood Obesity - microbiology Phylogeny Prospective Studies Relative abundance Risk factors Succinic Acid - blood Weight control |
| title | Elevated circulating levels of succinate in human obesity are linked to specific gut microbiota |
| url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T16%3A18%3A07IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Elevated%20circulating%20levels%20of%20succinate%20in%20human%20obesity%20are%20linked%20to%20specific%20gut%20microbiota&rft.jtitle=The%20ISME%20Journal&rft.au=Serena,%20Carolina&rft.date=2018-07-01&rft.volume=12&rft.issue=7&rft.spage=1642&rft.epage=1657&rft.pages=1642-1657&rft.issn=1751-7362&rft.eissn=1751-7370&rft_id=info:doi/10.1038/s41396-018-0068-2&rft_dat=%3Cproquest_pubme%3E2059531457%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c578t-9473427475aa4a5f215ebe09cf86652f2bcd7bbca52b7b87b72fdcaaf868d59d3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2059531457&rft_id=info:pmid/29434314&rfr_iscdi=true |