Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure

Zhang, Xueying; Sukhchuluun, Gansukh; Bo, Tingbei; Chi, Qing-Sheng; Yang, Junjie; Chen, Bin; Zhang, Lei; Wang, Dehua

doi:10.1186/s40168-018-0473-9

Cited by 98 publications

(101 citation statements)

References 92 publications

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“…Huddling is a long conserved interactive behavioral strategy that many mammals use to maximize their survival in harsh environments. Zhang et al hypothesized that the ability of huddling to alter energy usage and thermoregulation could shape cecal microbiota in small mammals, such as voles [68]. In their study, voles were maintained either in a group where they could huddle or as separate individuals and exposed to warm (23 ± 1 C) and cold (4 ± 1 C) air temperature.…”

Section: Evidence That Temperature Can Influence the Composition And mentioning

confidence: 99%

Temperature as a modulator of the gut microbiome: what are the implications and opportunities for thermal medicine?

Hylander

Repasky

2019

International Journal of Hyperthermia

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There is substantial research being conducted on the relationships between the gut microbiome, the immune response and health and disease. Environmental temperature and heat stress are known to modify the gut microbiome. Changes in core temperature have been linked, in multiple phyla, to altered microbiome composition and function. This raises the question of whether local/regional or whole body thermal therapies which target tumors in the abdomen, peritoneal cavity, or pelvis influence the gut microbiome. To date, there is little information on whether thermal therapy exerts positive or negative effects on the microbiome. This is an intriguing question since there is growing interest in the immunological impact of various thermal therapies. The goal of this brief review is to highlight research on how environmental conditions, particularly temperature (internal as well as external temperatures) influences the gut microbiome. Given the potential for temperature shifts to modulate gut microbe function and composition, it is likely that various forms of thermal therapy, including hyperthermic intraperitoneal chemotherapy (HIPEC), deep regional, and whole body hyperthermia influence the microbiome in ways that are currently not appreciated. More research is needed to determine whether thermal therapy induced changes in the microbiome occur, and whether they are beneficial or detrimental to the host. Currently, although approaches to microbiome modification such as dietary intervention, fecal transfer, probiotics and prebiotics are being developed, the potential of temperature manipulation has, as yet, not been explored. Therefore, new research could reveal whether perturbations of the microbiome composition that have negative health consequences (dysbiosis) could be an important target for treatment by thermal medicine.

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Section: Evidence That Temperature Can Influence the Composition And mentioning

confidence: 99%

Temperature as a modulator of the gut microbiome: what are the implications and opportunities for thermal medicine?

Hylander

Repasky

2019

International Journal of Hyperthermia

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“…The supporting information plus the data, and R script for this manuscript can be found on Zenodo/Github (41). The full list of transplant studies used in this article can be found in the dataset on Zenodo/GitHub (41), and (10,26,31,35, in the bibliography below.…”

Section: Fundingmentioning

confidence: 99%

“…Recently, researchers have started to appreciate the intertwining nature of hostmicrobiome interactions. Evidence is mounting that hosts can shape the composition of their microbiome community (10), and that microbiomes can influence their host's behaviour (8) and physiology (5). Based on differing cases of how host and microbiome might interact, Foster et al (11) proposed four distinct models: 1) 'host control', in which the host unilaterally governs the composition of its microbiome; 2) 'symbiont control', in which the microbiome shapes the host phenotype; 3) 'open ecosystem', in which the host and microbiome do not interact; and 4) 'ecosystem on a leash', in which the host influences the microbiome by selecting upon microbial function rather than for specific microbial taxa.…”

mentioning

confidence: 99%

Into the wild: microbiome transplant studies need broader ecological reality

Greyson-Gaito¹,

Bartley²,

Cottenie³

et al. 2019

Preprint

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Gut microbial communities (microbiomes) profoundly shape the ecology and evolution of multicellular life. Interactions between host and microbiome appear to be reciprocal, and ecological theory is now being applied to better understand how hosts and their microbiome influence each other. However, some ecological processes that underlie reciprocal host-microbiome interactions may be obscured by the current convention of highly-controlled transplantation experiments. Although these approaches have yielded invaluable insights, there is a need for a broader array of approaches to fully understand host-microbiome reciprocity. Using a directed review, we surveyed the breadth of ecological reality in the current literature on gut microbiome transplants with non-human recipients. For 55 studies, we categorized 9 key experimental conditions that impact the ecological reality (EcoReality) of the transplant, including host taxon match and donor environment. Using these categories, we rated the EcoReality of each transplant. Encouragingly, the breadth of EcoReality has increased over time, but some components of EcoReality are still relatively unexplored, including recipient host environment and microbiome state. The conceptual framework we develop here maps the landscape of possible EcoReality to highlight where fundamental ecological processes can be considered in future transplant experiments.

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“…It is a cooperative group behavior, permitting individuals involved in social thermoregulation to minimize heat loss and thereby lower energy expenditure, possibly allowing reallocation of saved energy to other functions [1,18]. It is commonly exhibited in small mammals and birds to reduce heat and energy loss under cold environments [19][20][21][22]. Research has shown that many mammals, such as degu (Octodon degus), Damaraland mole-rat (Cryptomys damarensis), and Natal mole-rat (C. hottentotus natalensis), huddle when the ambient temperature is lower than 15-20°C, with an energy saving of up to 30% [23,24].…”

Section: Introductionmentioning

confidence: 99%

“…Brandt's voles (Lasiopodomys brandtii) are small non-hibernating herbivorous rodents widely distributed in the Inner Mongolian grasslands of Northern China, dry steppe zone of Mongolia, and southeast Baikal region of Russia. They are highly socialized animals that huddle in winter as an adaptation to their harsh habitats [20]. Studies have shown that mild cooling can significantly change the level of oxidative stress in the cardiac muscle of Brandt's voles [29].…”

Section: Introductionmentioning

confidence: 99%

Huddling relieves myocardial glycogen synthesis of Brandt’s voles in mild cold environment

Wang¹,

Mou²,

Xu³

et al. 2020

Preprint

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Background:Small mammals have limited glucose use and limited glycogen accumulation during hypothermia. Huddling is a highly evolved cooperative behavioral strategy in social mammals, allowing adaptation to environmental cooling. As yet, however, is not clear whether this behavior affects the utilization of glycogen in cold environments. Here, we studied the effect of huddling on myocardial glycogen content in Brandt’s voles (Lasiopodomys brandtii) under a mild cold environment (15 °C). Results: Results showed that (1) Compared to the control (22 °C) group (CON), the number of glycogenosomes more than tripled in the cool separated group (CS) in both males and females; whereas the number of glycogenosomes increased in females but was maintained in males in the cool huddling group (CH). (2) The ratio of glycogen synthetase phosphorylation showed a similar trend as the change in glycogenosome number in the three treatment groups in both males and females. (3) Protein expression of glycogen phosphorylase remained stable in males in the three treatment groups but increased in CS group females compared with the CON group. Conclusion:These results indicate that huddling in voles alleviated the increase in myocardial glycogen content caused by the increase of glycogen synthesis under cool environments.

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Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure

Cited by 98 publications

References 92 publications

Temperature as a modulator of the gut microbiome: what are the implications and opportunities for thermal medicine?

Temperature as a modulator of the gut microbiome: what are the implications and opportunities for thermal medicine?

Into the wild: microbiome transplant studies need broader ecological reality

Huddling relieves myocardial glycogen synthesis of Brandt’s voles in mild cold environment

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