Seasonal restructuring of the ground squirrel gut microbiota over the annual hibernation cycle

Abstract

Many hibernating mammals suspend food intake during winter, relying solely on stored lipids to fuel metabolism. Winter fasting in these species eliminates a major source of degradable substrates to support growth of gut microbes, which may affect microbial community structure and host-microbial interactions. We explored the effect of the annual hibernation cycle on gut microbiotas using deep sequencing of 16S rRNA genes from ground squirrel cecal contents. Squirrel microbiotas were dominated by members of the phyla Bacteroidetes, Firmicutes, and Verrucomicrobia. UniFrac analysis showed that microbiotas clustered strongly by season, and maternal influences, diet history, host age, and host body temperature had minimal effects. Phylogenetic diversity and numbers of operational taxonomic units were lowest in late winter and highest in the spring after a 2-wk period of refeeding. Hibernation increased relative abundance of Bacteroidetes and Verrucomicrobia, phyla that contain species capable of surviving on host-derived substrates such as mucins, and reduced relative abundance of Firmicutes, many of which prefer dietary polysaccharides. Hibernation reduced cecal short-chain fatty acid and ammonia concentrations, and increased and decreased concentrations of acetate and butyrate, respectively. These results indicate that the ground squirrel microbiota is restructured each year in a manner that reflects differences in microbial preferences for dietary vs. host-derived substrates, and thus the competitive abilities of different taxa to survive in the altered environment in the hibernator gut.

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

“…The positive correlation between the butyrate concentration and Firmicutes relative abundance is not surprising, given that taxa within the Firmicutes are the primary butyrate producers in the gut (45). A similar correlation was found previously for active and hibernating thirteen-lined ground squirrels (10). Firmicutes relative abundance is correlated with diet-induced obesity in mice (20,24,25); however, no correlations between body condition and butyrate concentration or Firmicutes relative abundance were detected in this study.…”

“…Few studies have investigated the gut microbiota of hibernators (7)(8)(9), and even fewer have done so using modern techniques (i.e., 454 pyrosequencing) (10,11). Hibernation alters microbial diversity, dominant taxa, and metabolic production in thirteenlined ground squirrels (Ictidomys tridecemlineatus) (10) and arctic ground squirrels (11) compared to summer squirrels.…”

“…Hibernation alters microbial diversity, dominant taxa, and metabolic production in thirteenlined ground squirrels (Ictidomys tridecemlineatus) (10) and arctic ground squirrels (11) compared to summer squirrels. However, to our knowledge, no studies have described the gut microbiota of a hibernator across the active season or development.…”

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

“…Extended periods of host fasting likely select for microbes that are able to degrade and subsist on host-derived substrates such as mucins and other glycoproteins (2)(3)(4). Indeed, several studies have revealed a profound effect of fasting on the gut microbiota.…”

“…However, the Syrian hamster is a facultative hibernator that exhibits relatively short torpor bouts (3 to 4 days) and eats during IBAs, both of which may diminish effects of hibernation on the gut microbiota. Carey et al (4) were the first to survey the gut microbiota of an obligate seasonal hibernator, the thirteen-lined ground squirrel (TLS; Ictidomys tridecemlineatus), using next-generation DNA sequencing techniques. Their results clearly indicate significant seasonal changes in gut microbial diversity and composition.…”