Nitrogen recycling via gut symbionts increases in ground squirrels over the hibernation season

Abstract

Hibernation is a mammalian strategy that uses metabolic plasticity to reduce energy demands and enable long-term fasting. Fasting mitigates winter food scarcity but eliminates dietary nitrogen, jeopardizing body protein balance. Here, we reveal gut microbiome–mediated urea nitrogen recycling in hibernating thirteen-lined ground squirrels ( Ictidomys tridecemlineatus ). Ureolytic gut microbes incorporate urea nitrogen into metabolites that are absorbed by the host, with the nitrogen reincorporated into the squirrel’s protein pool. Urea nitrogen recycling is greatest after prolonged fasting in late winter, when urea transporter abundance in gut tissue and urease gene abundance in the microbiome are highest. These results reveal a functional role for the gut microbiome during hibernation and suggest mechanisms by which urea nitrogen recycling may contribute to protein balance in other monogastric animals.

Myostatin gene deletion alters gut microbiota stimulating fast-twitch glycolytic muscle growth

“…Moreover, the microbial metabolites–SCFAs treatment can also attenuate skeletal muscle impairments, especially in the GA muscle (Lahiri et al, 2019). During hibernation, the urease-producing microbes, Alistipes , enriched in the gut of ground squirrels can prevent muscle loss (Regan et al, 2022). These results strongly suggest that the intestinal flora remodeled by MSTN gene deletion is involved in the growth of fast-twitch glycolytic muscle mass and function, which may be related to the enrichment of SCFAs–producing microbes.…”

“…The intestinal microbiota plays a crucial role in muscle growth and development. For example, urease gene-rich microbes, Alistipes and Veillonella respectively maintain muscle mass in hibernating animals by promoting urea nitrogen salvage (Regan et al, 2022) and metabolize lactic acid to provide energy for skeletal muscles for long periods of exercise and increase endurance in runners (Scheiman et al, 2019). Short chain fatty acids (SCFAs) are gut microbiota-derived metabolites that are involved in maintaining the integrity of the intestinal mucosa, improving glucose and lipid metabolism, controlling energy expenditure, and regulating the immune system and inflammatory responses (Agus et al, 2021; Besten et al, 2013).…”

Functional and compositional changes in the fecal microbiome of a shorebird during pre-migratory weight gain

“…For example, arctic ground squirrels ( Urocitellus parryii) hibernate for 6-9 months and rely completely on the fat mass accumulated during their active season. Although the role of the microbiome in fattening is unknown in this species, the microbiome was recently shown to be involved in maintaining lean mass during hibernation [18]. In another hibernator, the brown bear ( Ursus arctos ), the microbiome undergoes annual changes.…”

Reshuffling of the coral microbiome during dormancy

“…In several hosts, including bears, squirrels, crickets and parasitoid wasps (Carey et al ., 2013; Sommer et al ., 2016; Dittmer and Brucker, 2021; Regan et al ., 2022), dormancy is associated with shifts in the composition of the host’s microbiome. One role these community shifts play may be to replace resource acquisition or use while host functioning is shut down or reduced (Carey et al ., 2013; Sommer et al ., 2016; Dittmer and Brucker, 2021; Regan et al ., 2022). For example, in ground squirrels, the restructuring of the gut is mediated by food availability (Carey et al ., 2013).…”

“…For example, in ground squirrels, the restructuring of the gut is mediated by food availability (Carey et al ., 2013). During hibernation the gut microbiome plays an important role in nitrogen recycling, while the squirrel is fasting (Regan et al ., 2022). Dormant states are also associated with pathogen avoidance, for example, nematodes enter diapause to avoid infection (e.g., by not ingesting pathogens; (Palominos et al ., 2017).…”