Seasonal Shifts in Gut Microbiota‐Mediated Nitrogen Recycling in 13‐Lined Ground Squirrels

Abstract

Hibernation is a complex phenotype that enables animals to fast for several months during periods of food scarcity. During this time, less of the hibernator's protein is degraded than would be predicted and, in the 13‐lined ground squirrel (Ictidomys tridecemlineatus), muscle volume and protein synthesis rise near the end of the hibernation season despite continued fasting and loss of body mass. With no exogenous nitrogen intake, one nitrogen source to support protein synthesis in late winter could be from urea nitrogen salvage (UNS), a nitrogen recycling process mediated by the ureolytic activity of the hibernator's gut microbiota. We hypothesized that the contribution of UNS to skeletal muscle growth in 13‐lined ground squirrels increases over the hibernation season, and tested this by comparing UNS processes in summer, early hibernation (1 month), and late hibernation (>3 months) squirrels. Data collected thus far suggest that expression of the urea transporter (UT‐B) in cecal tissue is 3‐fold greater in late winter than in summer squirrels (P<0.001; n=12 per group), indicating a greater capacity for transport of urea into the cecum during winter fasting. Real‐time measurement of microbial ureolytic activity using cavity ring‐down spectrometry on squirrels I.P.‐injected with 13C,15N‐labeled urea confirmed the bacterial origin of UNS, because δ13C in breath is substantially reduced in antibiotic‐depleted microbiotas. Isotope ratio mass spectrometry showed that tissues of squirrels treated with 13C,15N‐urea accumulated up to 200x more 15N as saline‐treated control squirrels, confirming that urea‐derived nitrogen is recycled and incorporated into host tissues. Together, these results corroborate UNS in active and hibernating 13‐lined ground squirrels and suggest that this mechanism for nitrogen recycling is a key aspect of the host‐microbe symbiosis in hibernating mammals that helps prepare the squirrels for spring emergence.Support or Funding InformationThis work is supported by NSF award IOS1558044This abstract is from the Experimental Biology 2019 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.