Temporal Dynamics of the Cecal Gut Microbiota of Juvenile Arctic Ground Squirrels: a Strong Litter Effect across the First Active Season

Abstract

Arctic ground squirrels (Urocitellus parryii) are active for a scant 3 to 5 months of the year. During the active season, adult squirrels compete for mates, reproduce, and fatten in preparation for hibernation, while juvenile squirrels, weaned in early July, must grow and acquire sufficient fat to survive their first hibernation season. During hibernation, the gut microbial community is altered in diversity, abundance, and activity. To date, no studies have examined the gut microbiota of hibernators across the truncated active season. We characterized trends in diversity (454 pyrosequencing), density (flow cytometry), viability (flow cytometry), and metabolism (short-chain fatty acid analysis) of the gut microbial community of juvenile arctic ground squirrels across their first active season at weaning and at 4, 6, 8, and 10 weeks postweaning. At 8 weeks postweaning, the mean bacterial density was significantly higher than that at weaning, and the mean percentage of live bacteria was significantly higher than that at either weaning or 4 weeks postweaning. No significant differences in microbial diversity, total short-chain fatty acid concentrations, or molar proportions of individual short-chain fatty acids were observed among sample periods. The level of variability in gut microbial diversity among squirrels was high across the active season but was most similar among littermates, except at weaning, indicating strong maternal or genetic influences across development. Our results indicate that genetic or maternal influences exert profound effects on the gut microbial community of juvenile arctic ground squirrels. We did not find a correlation between host adiposity and gut microbial diversity during prehibernation fattening, likely due to a high level of variability among squirrels.

Effects of microcystin-LR on gut microflora in different gut regions of mice

“…However, no significant variation was detected in the jejuno-ileum. Host disease as well as some toxic agents has been shown to decrease gut microbial diversity (Ling et al, 2014;Stevenson et al, 2014;Wu et al, 2014). Unexpectedly, in our study, the hepatotoxic MC-LR increased the gut microbial diversity.…”

Animal-microbial symbioses in changing environments

“…Some groups were nearly absent during hibernation, such as Lactobacillus . Similar patterns were observed in studies with hibernating arctic ground squirrels (Duddleston et al, 2012; Stevenson, 2014). These results suggest that competition for the limited amount of usable substrates in the hibernator gut may drive the altered microbial communities that emerge by late winter.…”

“…In hibernating thirteen-lined ground squirrels concentrations of total SCFAs in cecal fluid are about 75% lower relative to the active season when animals are feeding (Carey et al, 2013). Similar results were also observed in arctic ground squirrels hibernating at T b <0°C (Duddleston et al, 2012; Stevenson, 2014). Interpretation of these static measurements is limited without flux analyses that can estimate relative rates of SCFA production and disappearance (i.e., absorption and excretion).…”

“…Compared with active season squirrels, gut microbes of hibernators have access only to endogenous, host-derived substrates - primarily glycans and proteins found in mucins and sloughed epithelial cells (Johansson et al, 2011). Although enzyme activity is relatively slow at the low temperatures of deep torpor (<10 °C), host-derived substrates can be rapidly degraded during interbout arousals and result in production of SCFAs and other microbial metabolites (Carey et al, 2013; Duddleston et al, 2012; Stevenson, 2014). …”

Effects of Season and Host Physiological State on the Diversity, Density, and Activity of the Arctic Ground Squirrel Cecal Microbiota

“…Specifically, alpha diversity was lower, and beta diversity and composition differed in gut microbiotas of torpid, IBA, and posthibernation squirrels from those of summer squirrels. That hibernation is a physiological state that induces a significant alteration of the gut microbiota of AGSs is further supported by similarities between the summer microbiotas of adult AGSs characterized in this study and those of captive juvenile AGSs across their first active season, prior to their first hibernation season (32). We found evidence of a core hibernation microbiota in AGSs, and characteristics of the gut microbiota of AGSs during hibernation are similar to those described for TLSs (4), strongly suggestive of a core hibernation microbiota in obligate seasonal hibernators.…”