Gut Microbiota and Host Thermoregulation in Response to Ambient Temperature Fluctuations Saeid Khakisahneh, a,b Xue-Ying Zhang, a,b Zahra Nouri, a,b De-Hua Wang a,b a State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China b CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China Saeid Khakisahneh and Xue-Ying Zhang contributed equally to this work. Author order was determined both alphabetically and in order of increasing seniority. ABSTRACT Ambient temperature (T a ) is an important factor in shaping phenotypic plasticity. Plasticity is generally beneficial for animals in adapting to their environ- ments. Gut microbiota are crucial in regulating host physiological and behavioral processes. However, whether the gut microbiota play a role in regulating host phe- notypic plasticity under the conditions of repeated fluctuations in environmental fac- tors has rarely been examined. We used intermittent T a acclimations to test the hy- pothesis that the plasticity of gut microbiota confers on the host a metabolic adaptation to T a fluctuations. Mongolian gerbils (Meriones unguiculatus) were accli- mated to intermittent 5°C to 23°C, 37°C to 23°C or 23°C to 23°C conditions for 3 cy- cles (totally 3 months). Intermittent T a acclimations induced variations in resting metabolic rate (RMR), serum thyroid hormones, and core body temperature (T b ). We further identified that the -diversity of the microbial community varied with T a and showed diverse responses during the 3 cycles. Some specific bacteria were more sensitive to T a and were associated with host dynamic metabolic plasticity during T a acclimations. In addition, depletion of gut microbiota in antibiotic-treated gerbils im- paired metabolic plasticity, particularly at low T a , whereas supplementation with pro- pionate as an energy resource improved the inhibited thermogenic capacity and in- creased the survival rate in the cold. These findings demonstrate that both gut microbiota and their host were more adaptive after repeated acclimations, and dy- namic gut microbiota and their metabolites may confer host plasticity in thermoreg- ulation in response to T a fluctuations. It also implies that low T a 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 exam- ined. The present study, through an intermittent temperature acclimation model, in- dicates 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. Further- more, low temperature seems to be a crucial cue in driving the symbiosis between mammals and their gut microbiota during evolution. KEYWORDS food intake, gut microbiome, intermittent temperature, resting metabolic rate, thyroid hormones P henotypic plasticity is a vital adaptation of organisms to complex, variable envi- ronments, and it determines the fitness and distribution range of species (1, 2). Ambient temperature (T a ) is an important factor for shaping phenotypic plasticity in small mammals in the temperate and Arctic regions, which are characterized by fluctuating T a (3). A critical physiological adaptive strategy to cope with T a fluctuations Citation Khakisahneh S, Zhang X-Y, Nouri Z, Wang D-H. 2020. Gut microbiota and host thermoregulation in response to ambient temperature fluctuations. mSystems 5: e00514-20. https://doi.org/10.1128/ mSystems.00514-20. Editor Thomas J. Sharpton, Oregon State University Copyright © 2020 Khakisahneh et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Address correspondence to De-Hua Wang, wangdh@ioz.ac.cn. Received 10 June 2020 Accepted 30 September 2020 Published RESEARCH ARTICLE Host-Microbe Biology crossm September/October 2020 Volume 5 Issue 5 e00514-20 msystems.asm.org 1 20 October 2020 Downloaded from https://journals.asm.org/journal/msystems on 29 September 2021 by 34.228.166.90.