Taxonomic and Functional Fecal Microbiota Signatures Associated With Insulin Resistance in Non-Diabetic Subjects With Overweight/Obesity Within the Frame of the PREDIMED-Plus Study

ObjectiveAn altered gut microbiota has been associated with insulin resistance, a metabolic dysfunction consisting of cellular insulin signaling impairment. The aim of the present study is to determine the taxonomic and functional fecal microbiota signatures associated with HOMA-IR index in a popula...

Full description

Bibliographic Details
Main Authors: Alessandro Atzeni, Thomaz F. S. Bastiaanssen, John F. Cryan, Francisco J. Tinahones, Jesús Vioque, Dolores Corella, Montserrat Fitó, Josep Vidal, Isabel Moreno-Indias, Ana M. Gómez-Pérez, Laura Torres-Collado, Oscar Coltell, Olga Castañer, Monica Bulló, Jordi Salas-Salvadó
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-04-01
Series:Frontiers in Endocrinology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fendo.2022.804455/full
_version_ 1811288664408326144
author Alessandro Atzeni
Alessandro Atzeni
Alessandro Atzeni
Thomaz F. S. Bastiaanssen
John F. Cryan
Francisco J. Tinahones
Francisco J. Tinahones
Jesús Vioque
Jesús Vioque
Dolores Corella
Dolores Corella
Montserrat Fitó
Montserrat Fitó
Josep Vidal
Josep Vidal
Isabel Moreno-Indias
Isabel Moreno-Indias
Ana M. Gómez-Pérez
Ana M. Gómez-Pérez
Laura Torres-Collado
Laura Torres-Collado
Oscar Coltell
Oscar Coltell
Olga Castañer
Olga Castañer
Monica Bulló
Monica Bulló
Monica Bulló
Jordi Salas-Salvadó
Jordi Salas-Salvadó
Jordi Salas-Salvadó
author_facet Alessandro Atzeni
Alessandro Atzeni
Alessandro Atzeni
Thomaz F. S. Bastiaanssen
John F. Cryan
Francisco J. Tinahones
Francisco J. Tinahones
Jesús Vioque
Jesús Vioque
Dolores Corella
Dolores Corella
Montserrat Fitó
Montserrat Fitó
Josep Vidal
Josep Vidal
Isabel Moreno-Indias
Isabel Moreno-Indias
Ana M. Gómez-Pérez
Ana M. Gómez-Pérez
Laura Torres-Collado
Laura Torres-Collado
Oscar Coltell
Oscar Coltell
Olga Castañer
Olga Castañer
Monica Bulló
Monica Bulló
Monica Bulló
Jordi Salas-Salvadó
Jordi Salas-Salvadó
Jordi Salas-Salvadó
author_sort Alessandro Atzeni
collection DOAJ
description ObjectiveAn altered gut microbiota has been associated with insulin resistance, a metabolic dysfunction consisting of cellular insulin signaling impairment. The aim of the present study is to determine the taxonomic and functional fecal microbiota signatures associated with HOMA-IR index in a population with high cardiovascular risk.MethodsA total of 279 non-diabetic individuals (55–75 years aged) with overweight/obesity and metabolic syndrome were stratified according to tertiles of HOMA-IR index. Blood biochemical parameters, anthropometric measurements and fecal samples were collected at baseline. Fecal microbial DNA extraction, 16S amplicon sequencing and bioinformatics analysis were performed.ResultsDesulfovibrio, Odoribacter and Oscillospiraceae UCG-002 were negatively associated with HOMA-IR index, whereas predicted total functional abundances revealed gut metabolic modules mainly linked to amino acid degradation. Butyricicoccus, Erysipelotrichaceae UCG-003, Faecalibacterium were positively associated with HOMA-IR index, whereas predicted total functional abundances revealed gut metabolic modules mainly linked to saccharide degradation. These bacteria contribute differentially to the gut metabolic modules, being the degree of contribution dependent on insulin resistance. Both taxa and gut metabolic modules negatively associated to HOMA-IR index were linked to mechanisms involving sulfate reducing bacteria, improvement of intestinal gluconeogenesis and production of acetate. Furthermore, both taxa and gut metabolic modules positively associated to HOMA-IR index were linked to production and mechanisms of action of butyrate.ConclusionsSpecific taxonomic and functional fecal microbiota signatures associated with insulin resistance were identified in a non-diabetic population with overweight/obesity at high cardiovascular risk. These findings suggest that tailoring therapies based on specific fecal microbiota profiles could be a potential strategy to improve insulin sensitivity.
first_indexed 2024-04-13T03:40:09Z
format Article
id doaj.art-4a1cc03779584d05b802dadd33306d5f
institution Directory Open Access Journal
issn 1664-2392
language English
last_indexed 2024-04-13T03:40:09Z
publishDate 2022-04-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Endocrinology
spelling doaj.art-4a1cc03779584d05b802dadd33306d5f2022-12-22T03:04:10ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922022-04-011310.3389/fendo.2022.804455804455Taxonomic and Functional Fecal Microbiota Signatures Associated With Insulin Resistance in Non-Diabetic Subjects With Overweight/Obesity Within the Frame of the PREDIMED-Plus StudyAlessandro Atzeni0Alessandro Atzeni1Alessandro Atzeni2Thomaz F. S. Bastiaanssen3John F. Cryan4Francisco J. Tinahones5Francisco J. Tinahones6Jesús Vioque7Jesús Vioque8Dolores Corella9Dolores Corella10Montserrat Fitó11Montserrat Fitó12Josep Vidal13Josep Vidal14Isabel Moreno-Indias15Isabel Moreno-Indias16Ana M. Gómez-Pérez17Ana M. Gómez-Pérez18Laura Torres-Collado19Laura Torres-Collado20Oscar Coltell21Oscar Coltell22Olga Castañer23Olga Castañer24Monica Bulló25Monica Bulló26Monica Bulló27Jordi Salas-Salvadó28Jordi Salas-Salvadó29Jordi Salas-Salvadó30Department of Biochemistry and Biotechnology, Universitat Rovira i Virgili, Reus, SpainInstitut D’Investigació Sanitària Pere Virgili (IISPV), Hospital Universitari de Sant Joan de Reus, Reus, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainAPC Microbiome Ireland, Department of Anatomy and Neuroscience, University College Cork, Cork, IrelandAPC Microbiome Ireland, Department of Anatomy and Neuroscience, University College Cork, Cork, IrelandCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainUnidad de Gestión Clínica de Endocrinología y Nutrición, Instituto de Investigación Biomédica de Málaga (IBIMA), Hospital Universitario Virgen de la Victoria, Málaga, SpainInstituto de Investigación Sanitaria y Biomédica de Alicante, ISABIAL-Universidad Miguel Hernández (UMH), Alicante, SpainCentro de Investigación Biomédica en Red Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III (ISCIII), Madrid, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainDepartment of Preventive Medicine, University of Valencia, Valencia, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainCardiovascular Risk and Nutrition (Regicor Study Group), Hospital del Mar Research Institute (IMIM), Barcelona, Spain0Endocrinology and Nutrition Department, Institut d’Investigacions Biomèdiques August Pi Sunyer (IDIBAPS), Hospital Clinic Universitari, Barcelona, Spain1Centro de Investigación Biomédica en Red Diabetes y Enfermedades Metabólicas (CIBERDEM), Instituto de Salud Carlos III (ISCIII), Madrid, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainUnidad de Gestión Clínica de Endocrinología y Nutrición, Instituto de Investigación Biomédica de Málaga (IBIMA), Hospital Universitario Virgen de la Victoria, Málaga, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainUnidad de Gestión Clínica de Endocrinología y Nutrición, Instituto de Investigación Biomédica de Málaga (IBIMA), Hospital Universitario Virgen de la Victoria, Málaga, SpainInstituto de Investigación Sanitaria y Biomédica de Alicante, ISABIAL-Universidad Miguel Hernández (UMH), Alicante, SpainCentro de Investigación Biomédica en Red Epidemiología y Salud Pública (CIBERESP), Instituto de Salud Carlos III (ISCIII), Madrid, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, Spain2Department of Computer Languages and Systems, University Jaume I, Castelló de la Plana, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainCardiovascular Risk and Nutrition (Regicor Study Group), Hospital del Mar Research Institute (IMIM), Barcelona, SpainDepartment of Biochemistry and Biotechnology, Universitat Rovira i Virgili, Reus, SpainInstitut D’Investigació Sanitària Pere Virgili (IISPV), Hospital Universitari de Sant Joan de Reus, Reus, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainDepartment of Biochemistry and Biotechnology, Universitat Rovira i Virgili, Reus, SpainInstitut D’Investigació Sanitària Pere Virgili (IISPV), Hospital Universitari de Sant Joan de Reus, Reus, SpainCentro de Investigación Biomédica en Red de Fisiopatología de la Obesidad y la Nutrición (CIBEROBN), Instituto de Salud Carlos III, Madrid, SpainObjectiveAn altered gut microbiota has been associated with insulin resistance, a metabolic dysfunction consisting of cellular insulin signaling impairment. The aim of the present study is to determine the taxonomic and functional fecal microbiota signatures associated with HOMA-IR index in a population with high cardiovascular risk.MethodsA total of 279 non-diabetic individuals (55–75 years aged) with overweight/obesity and metabolic syndrome were stratified according to tertiles of HOMA-IR index. Blood biochemical parameters, anthropometric measurements and fecal samples were collected at baseline. Fecal microbial DNA extraction, 16S amplicon sequencing and bioinformatics analysis were performed.ResultsDesulfovibrio, Odoribacter and Oscillospiraceae UCG-002 were negatively associated with HOMA-IR index, whereas predicted total functional abundances revealed gut metabolic modules mainly linked to amino acid degradation. Butyricicoccus, Erysipelotrichaceae UCG-003, Faecalibacterium were positively associated with HOMA-IR index, whereas predicted total functional abundances revealed gut metabolic modules mainly linked to saccharide degradation. These bacteria contribute differentially to the gut metabolic modules, being the degree of contribution dependent on insulin resistance. Both taxa and gut metabolic modules negatively associated to HOMA-IR index were linked to mechanisms involving sulfate reducing bacteria, improvement of intestinal gluconeogenesis and production of acetate. Furthermore, both taxa and gut metabolic modules positively associated to HOMA-IR index were linked to production and mechanisms of action of butyrate.ConclusionsSpecific taxonomic and functional fecal microbiota signatures associated with insulin resistance were identified in a non-diabetic population with overweight/obesity at high cardiovascular risk. These findings suggest that tailoring therapies based on specific fecal microbiota profiles could be a potential strategy to improve insulin sensitivity.https://www.frontiersin.org/articles/10.3389/fendo.2022.804455/fullfecal microbiotainsulin resisitanceHOMA-IR16S sequencinggut metabolic modules
spellingShingle Alessandro Atzeni
Alessandro Atzeni
Alessandro Atzeni
Thomaz F. S. Bastiaanssen
John F. Cryan
Francisco J. Tinahones
Francisco J. Tinahones
Jesús Vioque
Jesús Vioque
Dolores Corella
Dolores Corella
Montserrat Fitó
Montserrat Fitó
Josep Vidal
Josep Vidal
Isabel Moreno-Indias
Isabel Moreno-Indias
Ana M. Gómez-Pérez
Ana M. Gómez-Pérez
Laura Torres-Collado
Laura Torres-Collado
Oscar Coltell
Oscar Coltell
Olga Castañer
Olga Castañer
Monica Bulló
Monica Bulló
Monica Bulló
Jordi Salas-Salvadó
Jordi Salas-Salvadó
Jordi Salas-Salvadó
Taxonomic and Functional Fecal Microbiota Signatures Associated With Insulin Resistance in Non-Diabetic Subjects With Overweight/Obesity Within the Frame of the PREDIMED-Plus Study
Frontiers in Endocrinology
fecal microbiota
insulin resisitance
HOMA-IR
16S sequencing
gut metabolic modules
title Taxonomic and Functional Fecal Microbiota Signatures Associated With Insulin Resistance in Non-Diabetic Subjects With Overweight/Obesity Within the Frame of the PREDIMED-Plus Study
title_full Taxonomic and Functional Fecal Microbiota Signatures Associated With Insulin Resistance in Non-Diabetic Subjects With Overweight/Obesity Within the Frame of the PREDIMED-Plus Study
title_fullStr Taxonomic and Functional Fecal Microbiota Signatures Associated With Insulin Resistance in Non-Diabetic Subjects With Overweight/Obesity Within the Frame of the PREDIMED-Plus Study
title_full_unstemmed Taxonomic and Functional Fecal Microbiota Signatures Associated With Insulin Resistance in Non-Diabetic Subjects With Overweight/Obesity Within the Frame of the PREDIMED-Plus Study
title_short Taxonomic and Functional Fecal Microbiota Signatures Associated With Insulin Resistance in Non-Diabetic Subjects With Overweight/Obesity Within the Frame of the PREDIMED-Plus Study
title_sort taxonomic and functional fecal microbiota signatures associated with insulin resistance in non diabetic subjects with overweight obesity within the frame of the predimed plus study
topic fecal microbiota
insulin resisitance
HOMA-IR
16S sequencing
gut metabolic modules
url https://www.frontiersin.org/articles/10.3389/fendo.2022.804455/full
work_keys_str_mv AT alessandroatzeni taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT alessandroatzeni taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT alessandroatzeni taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT thomazfsbastiaanssen taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT johnfcryan taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT franciscojtinahones taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT franciscojtinahones taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT jesusvioque taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT jesusvioque taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT dolorescorella taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT dolorescorella taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT montserratfito taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT montserratfito taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT josepvidal taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT josepvidal taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT isabelmorenoindias taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT isabelmorenoindias taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT anamgomezperez taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT anamgomezperez taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT lauratorrescollado taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT lauratorrescollado taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT oscarcoltell taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT oscarcoltell taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT olgacastaner taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT olgacastaner taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT monicabullo taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT monicabullo taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT monicabullo taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT jordisalassalvado taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT jordisalassalvado taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy
AT jordisalassalvado taxonomicandfunctionalfecalmicrobiotasignaturesassociatedwithinsulinresistanceinnondiabeticsubjectswithoverweightobesitywithintheframeofthepredimedplusstudy