Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations

ABSTRACT Ambient temperature (Ta) is an important factor in shaping phenotypic plasticity. Plasticity is generally beneficial for animals in adapting to their environments. Gut microbiota are crucial in regulating host physiological and behavioral processes. However, whether the gut microbiota play...

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Autores principales:	Saeid Khakisahneh, Xue-Ying Zhang, Zahra Nouri, De-Hua Wang
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	food intake gut microbiome intermittent temperature resting metabolic rate thyroid hormones Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5eea290caa674bf284e861b16c3fd3f5
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spelling	oai:doaj.org-article:5eea290caa674bf284e861b16c3fd3f52021-12-02T18:44:36ZGut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations10.1128/mSystems.00514-202379-5077https://doaj.org/article/5eea290caa674bf284e861b16c3fd3f52020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00514-20https://doaj.org/toc/2379-5077ABSTRACT Ambient temperature (Ta) is an important factor in shaping phenotypic plasticity. Plasticity is generally beneficial for animals in adapting to their environments. Gut microbiota are crucial in regulating host physiological and behavioral processes. However, whether the gut microbiota play a role in regulating host phenotypic plasticity under the conditions of repeated fluctuations in environmental factors has rarely been examined. We used intermittent Ta acclimations to test the hypothesis that the plasticity of gut microbiota confers on the host a metabolic adaptation to Ta fluctuations. Mongolian gerbils (Meriones unguiculatus) were acclimated to intermittent 5°C to 23°C, 37°C to 23°C or 23°C to 23°C conditions for 3 cycles (totally 3 months). Intermittent Ta acclimations induced variations in resting metabolic rate (RMR), serum thyroid hormones, and core body temperature (Tb). We further identified that the β-diversity of the microbial community varied with Ta and showed diverse responses during the 3 cycles. Some specific bacteria were more sensitive to Ta and were associated with host dynamic metabolic plasticity during Ta acclimations. In addition, depletion of gut microbiota in antibiotic-treated gerbils impaired metabolic plasticity, particularly at low Ta, whereas supplementation with propionate as an energy resource improved the inhibited thermogenic capacity and increased the survival rate in the cold. These findings demonstrate that both gut microbiota and their host were more adaptive after repeated acclimations, and dynamic gut microbiota and their metabolites may confer host plasticity in thermoregulation in response to Ta fluctuations. It also implies that low Ta is a crucial cue in driving symbiosis between mammals and their gut microbiota during evolution. IMPORTANCE Whether gut microbiota play a role in regulating host phenotypic plasticity in small mammals living in seasonal environments has rarely been examined. The present study, through an intermittent temperature acclimation model, indicates that both gut microbiota and their host were more adaptive after repeated acclimations. It also demonstrates that dynamic gut microbiota confer host plasticity in thermoregulation in response to intermittent temperature fluctuations. Furthermore, low temperature seems to be a crucial cue in driving the symbiosis between mammals and their gut microbiota during evolution.Saeid KhakisahnehXue-Ying ZhangZahra NouriDe-Hua WangAmerican Society for Microbiologyarticlefood intakegut microbiomeintermittent temperatureresting metabolic ratethyroid hormonesMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	food intake gut microbiome intermittent temperature resting metabolic rate thyroid hormones Microbiology QR1-502
spellingShingle	food intake gut microbiome intermittent temperature resting metabolic rate thyroid hormones Microbiology QR1-502 Saeid Khakisahneh Xue-Ying Zhang Zahra Nouri De-Hua Wang Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations
description	ABSTRACT Ambient temperature (Ta) is an important factor in shaping phenotypic plasticity. Plasticity is generally beneficial for animals in adapting to their environments. Gut microbiota are crucial in regulating host physiological and behavioral processes. However, whether the gut microbiota play a role in regulating host phenotypic plasticity under the conditions of repeated fluctuations in environmental factors has rarely been examined. We used intermittent Ta acclimations to test the hypothesis that the plasticity of gut microbiota confers on the host a metabolic adaptation to Ta fluctuations. Mongolian gerbils (Meriones unguiculatus) were acclimated to intermittent 5°C to 23°C, 37°C to 23°C or 23°C to 23°C conditions for 3 cycles (totally 3 months). Intermittent Ta acclimations induced variations in resting metabolic rate (RMR), serum thyroid hormones, and core body temperature (Tb). We further identified that the β-diversity of the microbial community varied with Ta and showed diverse responses during the 3 cycles. Some specific bacteria were more sensitive to Ta and were associated with host dynamic metabolic plasticity during Ta acclimations. In addition, depletion of gut microbiota in antibiotic-treated gerbils impaired metabolic plasticity, particularly at low Ta, whereas supplementation with propionate as an energy resource improved the inhibited thermogenic capacity and increased the survival rate in the cold. These findings demonstrate that both gut microbiota and their host were more adaptive after repeated acclimations, and dynamic gut microbiota and their metabolites may confer host plasticity in thermoregulation in response to Ta fluctuations. It also implies that low Ta is a crucial cue in driving symbiosis between mammals and their gut microbiota during evolution. IMPORTANCE Whether gut microbiota play a role in regulating host phenotypic plasticity in small mammals living in seasonal environments has rarely been examined. The present study, through an intermittent temperature acclimation model, indicates that both gut microbiota and their host were more adaptive after repeated acclimations. It also demonstrates that dynamic gut microbiota confer host plasticity in thermoregulation in response to intermittent temperature fluctuations. Furthermore, low temperature seems to be a crucial cue in driving the symbiosis between mammals and their gut microbiota during evolution.
format	article
author	Saeid Khakisahneh Xue-Ying Zhang Zahra Nouri De-Hua Wang
author_facet	Saeid Khakisahneh Xue-Ying Zhang Zahra Nouri De-Hua Wang
author_sort	Saeid Khakisahneh
title	Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations
title_short	Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations
title_full	Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations
title_fullStr	Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations
title_full_unstemmed	Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations
title_sort	gut microbiota and host thermoregulation in response to ambient temperature fluctuations
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/5eea290caa674bf284e861b16c3fd3f5
work_keys_str_mv	AT saeidkhakisahneh gutmicrobiotaandhostthermoregulationinresponsetoambienttemperaturefluctuations AT xueyingzhang gutmicrobiotaandhostthermoregulationinresponsetoambienttemperaturefluctuations AT zahranouri gutmicrobiotaandhostthermoregulationinresponsetoambienttemperaturefluctuations AT dehuawang gutmicrobiotaandhostthermoregulationinresponsetoambienttemperaturefluctuations
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Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations

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