BackgroundHuddling is highly evolved as a cooperative behavioral strategy for social mammals to maximize their fitness in harsh environments. Huddling behavior can change psychological and physiological responses. The coevolution of mammals with their microbial communities confers fitness benefits to both partners. The gut microbiome is a key regulator of host immune and metabolic functions. We hypothesized that huddling behavior altered energetics and thermoregulation by shaping caecal microbiota in small herbivores. Brandt’s voles (Lasiopodomys brandtii) were maintained in a group (huddling) or as individuals (separated) and were exposed to warm (23 ± 1 °C) and cold (4 ± 1 °C) air temperatures (Ta).ResultsVoles exposed to cold Ta had higher energy intake, resting metabolic rate (RMR) and nonshivering thermogenesis (NST) than voles exposed to warm Ta. Huddling voles had lower RMR and NST than separated voles in cold. In addition, huddling voles had a higher surface body temperature (Tsurface), but lower core body temperature (Tcore) than separated voles, suggesting a lower set-point of Tcore in huddling voles. Both cold and huddling induced a marked variation in caecal bacterial composition, which was associated with the lower Tcore. Huddling voles had a higher α and β-diversity, abundance of Lachnospiraceae and Veillonellaceae, but lower abundance of Cyanobacteria, Tenericutes, TM7, Comamonadaceae, and Sinobacteraceae than separated voles. Huddling or cold resulted in higher concentrations of short-chain fatty acids (SCFAs), particularly acetic acid and butyric acid when compared to their counterparts. Transplantation of caecal microbiota from cold-separated voles but not from cold-huddling voles induced significant increases in energy intake and RMR compared to that from warm-separated voles.ConclusionsThese findings demonstrate that the remodeling of gut microbiota, which is associated with a reduction in host Tcore, mediates cold- and huddling-induced energy intake and thermoregulation and therefore orchestrates host metabolic and thermal homeostasis. It highlights the coevolutionary mechanism of host huddling and gut microbiota in thermoregulation and energy saving for winter survival in endotherms.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0473-9) contains supplementary material, which is available to authorized users.

Many small mammals engage in coprophagy, or the behavior of consuming feces, as a means to meet nutritional requirements when feeding on low-quality foods. In addition to nutritional benefits, coprophagy may also help herbivores retain necessary gut microbial diversity and function, which may have downstream physiological effects, such as maintaining energy balance and cognitive function. Here, we used collars to prevent Brandt's vole (Lasiopodomys brandtii) from engaging in coprophagy and monitored changes in microbial community structure, energy metabolism, and cognitive performance. In this research, we found that coprophagy prevention decreased alpha diversity of the gut microbiota, and altered proportions of microbial taxa such as Bacteroidetes, Firmicutes, and Oscillospira. Preventing coprophagy resulted in a reduced body mass, and increased food intake. Importantly, coprophagy prevention decreased vole cognitive behavior and altered levels of neurotransmitters in brain. Daily acetate administration was able to reverse some of the coprophagy prevention-induced changes in microbiota composition, metabolism, neurochemistry, and cognitive behavior. These findings identify the functional importance of coprophagy behavior and interactions between the gut microbiota, energy metabolism, and neurological function. Our results suggest that coprophagy contributes to stabilizing the gut microbiota, promoting microbial metabolism, maintaining host energy balance and, consequently, altering cognitive performance.

Gut microbiota play a critical role in orchestrating metabolic homeostasis of the host. However, the crosstalk between host and microbial symbionts in small mammals are rarely illustrated. We used male Brandt's voles (Lasiopodomys brandtii) to test the hypothesis that gut microbiota and host neurotransmitters, such as norepinephrine (NE), interact to regulate energetics and thermogenesis during cold acclimation. We found that increases in food intake and thermogenesis were associated with increased monoamine neurotransmitters, ghrelin, short-chain fatty acids, and altered cecal microbiota during cold acclimation. Further, our pair-fed study showed that cold temperature can alter the cecal microbiota independently of overfeeding. Using cecal microbiota transplant along with β3-adrenoceptor antagonism and PKA inhibition, we confirmed that transplant of coldacclimated microbiota increased thermogenesis through activation of cAMP-PKA-pCREB signaling. In addition, NE manipulation induced a long-term alteration in gut microbiota structure. These data demonstrate that gut microbiota-NE crosstalk via cAMP signaling regulates energetics and thermogenesis during cold acclimation in male Brandt's voles.

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Human skin microbiota plays a crucial role in the defense against pathogens, and is associated with various skin diseases. High elevation is positively correlated with various extreme environmental conditions (i.e., high ultraviolet radiation), which may exert selection pressure on skin microbiota, and therefore influence human health. Most studies regarding skin microbial communities have focused on low-elevation hosts. Few studies have explored skin microbiota in high-elevation humans. Here, we investigated the diversity, function, assembly, and co-occurrence patterns of skin microbiotas from 35 health human subjects across three body sites (forehead, opisthenar, and palm) and seven elevation gradients from 501 to 3431 m. Alpha diversity values (i.e., Shannon diversity and observed operational taxonomic units (OTUs)) decreased with increasing elevation regardless of the body site, while beta diversity (Jaccard and Bray–Curtis dissimilarities) showed an increasing trend with elevation. Elevation is a significant factor that influences human skin microbiota, even after controlling host-related factors. Skin microbiotas at high elevation with more than 3000 m on the Qinghai–Tibet Plateau, had a significant structural or functional separation from those at low elevation with less than 3000 m. Notably, the clustering coefficient, average degree, and network density were all lower at high-elevation than those at low-elevation, suggesting that high-elevation skin networks were more fragile and less connected. Phylogenetic analysis showed that human skin microbiotas are mainly dominated by stochastic processes (58.4%–74.6%), but skin microbiotas at high-elevation harbor a greater portion of deterministic processes than those at low-elevation, indicating that high-elevation may be conducive to the promotion of deterministic processes. Our results reveal that the filtering and selection of the changeable high-elevation environment on the Qinghai–Tibet Plateau may lead to less stable skin microbial community structures.

Ambient temperature and food composition can affect energy metabolism of the host. Thermal transient receptor potential (thermo-TRPs) ion channels can detect temperature signals and are involved in the regulation of thermogenesis and energy homeostasis. Further, the gut microbiota has also been implicated in thermogenesis and obesity. In the present study, we tested the hypothesis that thermo-TRPs and gut microbiota are involved in reducing diet-induced obesity (DIO) during low temperature exposure. C57BL/6J mice in obese (body mass gain >45%), lean (body mass gain <15%), and control (body mass gain<1%) groups were exposed to high (23±1°C) or low (4±1°C) ambient temperature for 28 days. Our data showed that low temperature exposure attenuated DIO, but enhanced brown adipose tissue (BAT) thermogenesis. Low temperature exposure also resulted in increased norepinephrine (NE) concentrations in the hypothalamus, decreased TRP melastatin 8 (TRPM8) expression in the small intestine, and altered composition and diversity of gut microbiota. In DIO mice, there was a decrease in overall energy intake along with a reduction in TRP ankyrin 1 (TRPA1) expression and an increase in NE concentration in the small intestine. DIO mice also showed increases in Oscillospira, [Ruminococcus], Lactococcus, and Christensenella and decreases in Prevotella, Odoribacter, and Lactobacillus at the genus level in fecal samples. Together, our data suggest that thermos-TRPs and gut microbiota are involved in thermogenesis and energy metabolism during low temperature exposure in DIO mice.

Precocious puberty mostly stems from endocrine disorders. However, more and more studies show that a high-fat diet (HFD) is closely related to precocious puberty, but its mechanism is unknown. Since gut microbiota is associated with hormone secretion and obesity, it inspires us to detect the mechanism of gut microbiota in triggering precocious puberty. The model of precocious puberty was established by feeding female mice with an HFD from 21 days old. After puberty, the serum hormone levels, gut microbiome sequencing, and metabolomics were collected. DNA was extracted from feces, and the V3–V4 region of the bacterial 16S rRNA gene was amplified, followed by microbial composition analysis. Subsequently, associations between precocious puberty and the microbiota were determined. We found that (1) HFD after weaning caused precocious puberty, increased serum estradiol, leptin, deoxycholic acid (DCA), and gonadotropin-releasing hormone (GnRH) in the hypothalamus; (2) Through correlation analysis, we found that GnRH was positively correlated with Desulfovibrio, Lachnoclostridium, GCA-900066575, Streptococcus, Anaerotruncus, and Bifidobacterium, suggesting that these bacteria may have a role in promoting sexual development. (3) “HFD-microbiota” transplantation promoted the precocious puberty of mice. (4) Estrogen changes the composition and proportion of gut microbiota and promotes precocious puberty. Therefore, the effect of HFD on precocious puberty is regulated by the interaction of gut microbiota and hormones.

Ambient temperature considerably affects the physiology and behavior of mammals. Thermosensory and thermoregulatory abilities play an important role in the response to changing ambient temperature in endotherms. However, the molecular mechanisms of behavioral thermoregulation remain poorly understood. Transient receptor potential vanilloid‐1 (TRPV1) is activated by changes in ambient temperature and is involved in acute thermoregulation. Here, we aimed to determine whether TRPV1 is involved in behavioral thermoregulation in wild rodents by conducting 2 experiments. In the first, 42 adult Mongolian gerbils (Meriones unguiculatus; 14 per treatment) were randomly assigned to 3 housing temperatures (4, 23, and 36°C) for 4 weeks. In the second, 20 gerbils (10 per treatment) were randomly injected with capsaicin (TRPV1 agonist) or AMG517 (TRPV1 antagonist). The results showed a significant decrease in food intake and non‐shivering thermogenesis in the gerbils housed at 36°C. Additionally, there was a significant increase in the preference of gerbils housed at 4°C to low temperatures. The expression of TRPV1 protein in the brown adipose tissue (BAT) and liver was significantly positively correlated with that of protein kinase A (PKA). The expression of TRPV1 and PKA proteins in the BAT was positively correlated with the temperature preference of the gerbils. The gerbils injected with capsaicin preferred significantly lower temperatures than the control group gerbils. These findings suggest that TRPV1 and PKA are involved in behavioral thermoregulation in Mongolian gerbils.