Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status

Gonadal steroid hormones have been suggested as the underlying mechanism responsible for the sexual dimorphism observed in metabolic diseases. Animal studies have also evidenced a causal role of the gut microbiome and metabolic health. However, the role of sexual dimorphism in the gut microbiota and...

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Detalhes bibliográficos
Autores: Mayneris Perxachs, Jordi, Arnoriaga Rodríguez, María, Luque-Córdoba, Diego, Priego Capote, Feliciano, Pérez Brocal, Vicente, Moya, Andrés, Burokas, Aurelijus, Maldonado, Rafael, Fernández-Real Lemos, José Manuel
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2020
País:España
Recursos:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repositorio:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:10256/19486
Acesso em linha:http://hdl.handle.net/10256/19486
Access Level:acceso abierto
Palavra-chave:Intestins -- Microbiologia
Intestines -- Microbiology
Intestins -- Malalties
Intestines -- Diseases
Persones obeses
Overweight persons
Menopausa
Menopause
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oai_identifier_str oai:recercat.cat:10256/19486
network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status
title Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status
spellingShingle Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status
Mayneris Perxachs, Jordi
Intestins -- Microbiologia
Intestines -- Microbiology
Intestins -- Malalties
Intestines -- Diseases
Persones obeses
Overweight persons
Menopausa
Menopause
title_short Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status
title_full Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status
title_fullStr Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status
title_full_unstemmed Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status
title_sort Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal status
dc.creator.none.fl_str_mv Mayneris Perxachs, Jordi
Arnoriaga Rodríguez, María
Luque-Córdoba, Diego
Priego Capote, Feliciano
Pérez Brocal, Vicente
Moya, Andrés
Burokas, Aurelijus
Maldonado, Rafael
Fernández-Real Lemos, José Manuel
author Mayneris Perxachs, Jordi
author_facet Mayneris Perxachs, Jordi
Arnoriaga Rodríguez, María
Luque-Córdoba, Diego
Priego Capote, Feliciano
Pérez Brocal, Vicente
Moya, Andrés
Burokas, Aurelijus
Maldonado, Rafael
Fernández-Real Lemos, José Manuel
author_role author
author2 Arnoriaga Rodríguez, María
Luque-Córdoba, Diego
Priego Capote, Feliciano
Pérez Brocal, Vicente
Moya, Andrés
Burokas, Aurelijus
Maldonado, Rafael
Fernández-Real Lemos, José Manuel
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Intestins -- Microbiologia
Intestines -- Microbiology
Intestins -- Malalties
Intestines -- Diseases
Persones obeses
Overweight persons
Menopausa
Menopause
topic Intestins -- Microbiologia
Intestines -- Microbiology
Intestins -- Malalties
Intestines -- Diseases
Persones obeses
Overweight persons
Menopausa
Menopause
description Gonadal steroid hormones have been suggested as the underlying mechanism responsible for the sexual dimorphism observed in metabolic diseases. Animal studies have also evidenced a causal role of the gut microbiome and metabolic health. However, the role of sexual dimorphism in the gut microbiota and the potential role of the microbiome in influencing sex steroid hormones and shaping sexually dimorphic susceptibility to disease have been largely overlooked. Although there is some evidence of sex-specific differences in the gut microbiota diversity, composition, and functionality, the results are inconsistent. Importantly, most of these studies have not taken into account the gonadal steroid status. Therefore, we investigated the gut microbiome composition and functionality in relation to sex, menopausal status, and circulating sex steroids.Results No significant differences were found in alpha diversity indices among pre- and post-menopausal women and men, but beta diversity differed among groups. The gut microbiota from post-menopausal women was more similar to men than to pre-menopausal women. Metagenome functional analyses revealed no significant differences between post-menopausal women and men. Gonadal steroids were specifically associated with these differences. Hence, the gut microbiota of pre-menopausal women was more enriched in genes from the steroid biosynthesis and degradation pathways, with the former having the strongest fold change among all associated pathways. Microbial steroid pathways also had significant associations with the plasma levels of testosterone and progesterone. In addition, a specific microbiome signature was able to predict the circulating testosterone levels at baseline and after 1-year follow-up. In addition, this microbiome signature could be transmitted from humans to antibiotic-induced microbiome-depleted male mice, being able to predict donor’s testosterone levels 4 weeks later, implying that the microbiota profile of the recipient mouse was influenced by the donor’s gender. Finally, obesity eliminated most of the differences observed among non-obese pre-menopausal women, post-menopausal women, and men in the gut microbiota composition (Bray-Curtis and weighted unifrac beta diversity), functionality, and the gonadal steroid status. Conclusions The present findings evidence clear differences in the gut microbial composition and functionality between men and women, which is eliminated by both menopausal and obesity status. We also reveal a tight link between the gut microbiota composition and the circulating levels of gonadal steroids, particularly testosterone
publishDate 2020
dc.date.none.fl_str_mv 2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
peer-reviewed
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10256/19486
url http://hdl.handle.net/10256/19486
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1186/s40168-020-00913-x
info:eu-repo/semantics/altIdentifier/eissn/2049-2618
dc.rights.none.fl_str_mv Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv Attribution 4.0 International
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv Microbiome, 2020, vol. 8, art.núm. 136
Articles publicats (D-CM)
reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Gut microbiota steroid sexual dimorphism and its impact on gonadal steroids: influences of obesity and menopausal statusMayneris Perxachs, JordiArnoriaga Rodríguez, MaríaLuque-Córdoba, DiegoPriego Capote, FelicianoPérez Brocal, VicenteMoya, AndrésBurokas, AurelijusMaldonado, RafaelFernández-Real Lemos, José ManuelIntestins -- MicrobiologiaIntestines -- MicrobiologyIntestins -- MalaltiesIntestines -- DiseasesPersones obesesOverweight personsMenopausaMenopauseGonadal steroid hormones have been suggested as the underlying mechanism responsible for the sexual dimorphism observed in metabolic diseases. Animal studies have also evidenced a causal role of the gut microbiome and metabolic health. However, the role of sexual dimorphism in the gut microbiota and the potential role of the microbiome in influencing sex steroid hormones and shaping sexually dimorphic susceptibility to disease have been largely overlooked. Although there is some evidence of sex-specific differences in the gut microbiota diversity, composition, and functionality, the results are inconsistent. Importantly, most of these studies have not taken into account the gonadal steroid status. Therefore, we investigated the gut microbiome composition and functionality in relation to sex, menopausal status, and circulating sex steroids.Results No significant differences were found in alpha diversity indices among pre- and post-menopausal women and men, but beta diversity differed among groups. The gut microbiota from post-menopausal women was more similar to men than to pre-menopausal women. Metagenome functional analyses revealed no significant differences between post-menopausal women and men. Gonadal steroids were specifically associated with these differences. Hence, the gut microbiota of pre-menopausal women was more enriched in genes from the steroid biosynthesis and degradation pathways, with the former having the strongest fold change among all associated pathways. Microbial steroid pathways also had significant associations with the plasma levels of testosterone and progesterone. In addition, a specific microbiome signature was able to predict the circulating testosterone levels at baseline and after 1-year follow-up. In addition, this microbiome signature could be transmitted from humans to antibiotic-induced microbiome-depleted male mice, being able to predict donor’s testosterone levels 4 weeks later, implying that the microbiota profile of the recipient mouse was influenced by the donor’s gender. Finally, obesity eliminated most of the differences observed among non-obese pre-menopausal women, post-menopausal women, and men in the gut microbiota composition (Bray-Curtis and weighted unifrac beta diversity), functionality, and the gonadal steroid status. Conclusions The present findings evidence clear differences in the gut microbial composition and functionality between men and women, which is eliminated by both menopausal and obesity status. We also reveal a tight link between the gut microbiota composition and the circulating levels of gonadal steroids, particularly testosteroneThis work was partially supported by research grants FIS (PI15/01934) from the Instituto de Salud Carlos III from Spain, SAF2015-65878-R and AEISAF2017-84060-R from Ministry of Economy and Competitiveness, Prometeo/ 2018/A/133 from Generalitat Valenciana, Spain, and also by European Commission (FP7, NeuroPain #2013-602891; #H2020-SC1-2019-2-RTD-848099 (PAINFACT)), the Catalan Government (AGAUR, #SGR2017-669, ICREA Academia Award 2015), the Spanish Instituto de Salud Carlos III (RTA, #RD16/ 0017/0020), the Fondo Europeo de Desarrollo Regional (FEDER) through the Programa Interreg V-A España-Francia-Andorra (POCTEFA 2014-2020), and the European Regional Development Fund (project No. 01.2.2-LMT-K-718-02- 0014) under grant agreement with the Research Council of Lithuania (LMTLT). María Arnoriaga Rodríguez is funded by a predoctoral Río Hortega contract (CM19/00190, co-funded by European Social Fund “Investing in your future”) from the Instituto de Salud Carlos III, Spain. Jordi Mayneris-Perxachs is funded by the Miguel Servet Program from the Instituto de Salud Carlos III (ISCIII CP18/00009), co-funded by the European Social Fund “Investing in your future”BioMed Central2020info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionpeer-reviewedapplication/pdfhttp://hdl.handle.net/10256/19486Microbiome, 2020, vol. 8, art.núm. 136Articles publicats (D-CM)reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)Inglésinfo:eu-repo/semantics/altIdentifier/doi/10.1186/s40168-020-00913-xinfo:eu-repo/semantics/altIdentifier/eissn/2049-2618Attribution 4.0 Internationalhttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:10256/194862026-05-29T05:05:01Z
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