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Atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome

Trillions of microbial oscillators reside throughout the mammalian body, yet their contributions toward fundamental features of host circadian rhythms (CRs) have not been characterized. Here, we demonstrate that the microbiome contributes to host CRs in activity and thermoregulation. Mice devoid of...

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Autores principales: Leone, Vanessa A., Onishi, Kenneth G., Kennedy, Megan, Riggle, Jonathan P., Pierre, Joseph F., Maneval, Andrew C., Spedale, Melanie N., Theriault, Betty R., Chang, Eugene B., Prendergast, Brian J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9411200/
https://www.ncbi.nlm.nih.gov/pubmed/36008471
http://dx.doi.org/10.1038/s41598-022-18291-9
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author Leone, Vanessa A.
Onishi, Kenneth G.
Kennedy, Megan
Riggle, Jonathan P.
Pierre, Joseph F.
Maneval, Andrew C.
Spedale, Melanie N.
Theriault, Betty R.
Chang, Eugene B.
Prendergast, Brian J.
author_facet Leone, Vanessa A.
Onishi, Kenneth G.
Kennedy, Megan
Riggle, Jonathan P.
Pierre, Joseph F.
Maneval, Andrew C.
Spedale, Melanie N.
Theriault, Betty R.
Chang, Eugene B.
Prendergast, Brian J.
author_sort Leone, Vanessa A.
collection PubMed
description Trillions of microbial oscillators reside throughout the mammalian body, yet their contributions toward fundamental features of host circadian rhythms (CRs) have not been characterized. Here, we demonstrate that the microbiome contributes to host CRs in activity and thermoregulation. Mice devoid of microbes (germ-free, GF) exhibited higher-amplitude CRs in a light–dark cycle and longer circadian periods in constant darkness. Circadian entrainment to food was greater in GF mice, but resetting responses to simulated jet-lag were unaffected. Microbial transplantation with cecal contents of conventionally-raised mice normalized CRs of GF mice, indicating that the concurrent activity of gut microbes modulates host circadian networks. Obesogenic effects of high-fat diet were absent in GF mice, but some circadian-disruptive effects persisted. Transkingdom (host-microbe) interactions affect circadian period and entrainment of CRs in diverse traits, and microbes alter interactions among light- and food-entrainable circadian processes in the face of environmental (light, diet) perturbations.
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spelling pubmed-94112002022-08-27 Atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome Leone, Vanessa A. Onishi, Kenneth G. Kennedy, Megan Riggle, Jonathan P. Pierre, Joseph F. Maneval, Andrew C. Spedale, Melanie N. Theriault, Betty R. Chang, Eugene B. Prendergast, Brian J. Sci Rep Article Trillions of microbial oscillators reside throughout the mammalian body, yet their contributions toward fundamental features of host circadian rhythms (CRs) have not been characterized. Here, we demonstrate that the microbiome contributes to host CRs in activity and thermoregulation. Mice devoid of microbes (germ-free, GF) exhibited higher-amplitude CRs in a light–dark cycle and longer circadian periods in constant darkness. Circadian entrainment to food was greater in GF mice, but resetting responses to simulated jet-lag were unaffected. Microbial transplantation with cecal contents of conventionally-raised mice normalized CRs of GF mice, indicating that the concurrent activity of gut microbes modulates host circadian networks. Obesogenic effects of high-fat diet were absent in GF mice, but some circadian-disruptive effects persisted. Transkingdom (host-microbe) interactions affect circadian period and entrainment of CRs in diverse traits, and microbes alter interactions among light- and food-entrainable circadian processes in the face of environmental (light, diet) perturbations. Nature Publishing Group UK 2022-08-25 /pmc/articles/PMC9411200/ /pubmed/36008471 http://dx.doi.org/10.1038/s41598-022-18291-9 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Leone, Vanessa A.
Onishi, Kenneth G.
Kennedy, Megan
Riggle, Jonathan P.
Pierre, Joseph F.
Maneval, Andrew C.
Spedale, Melanie N.
Theriault, Betty R.
Chang, Eugene B.
Prendergast, Brian J.
Atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome
title Atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome
title_full Atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome
title_fullStr Atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome
title_full_unstemmed Atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome
title_short Atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome
title_sort atypical behavioral and thermoregulatory circadian rhythms in mice lacking a microbiome
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9411200/
https://www.ncbi.nlm.nih.gov/pubmed/36008471
http://dx.doi.org/10.1038/s41598-022-18291-9
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