Abstract
Mammalian herbivores rely on microbial activities in an expanded gut chamber to convert plant biomass into absorbable nutrients. Distinct from ruminants, small herbivores typically have a simple stomach but an enlarged cecum to harbor symbiotic microbes; however, knowledge of this specialized gut structure and characteristics of its microbial contents is limited. Here, we used leaf-eating flying squirrels as a model to explore functional characteristics of the cecal microbiota adapted to a high-fiber, toxin-rich diet. Specifically, environmental conditions across gut regions were evaluated by measuring mass, pH, feed particle size, and metabolomes. Then, parallel metagenomes and metatranscriptomes were used to detect microbial functions corresponding to the cecal environment. Based on metabolomic profiles, >600 phytochemical compounds were detected, although many were present only in the foregut and probably degraded or transformed by gut microbes in the hindgut. Based on metagenomic (DNA) and metatranscriptomic (RNA) profiles, taxonomic compositions of the cecal microbiota were dominated by bacteria of the Firmicutes taxa; they contained major gene functions related to degradation and fermentation of leaf-derived compounds. Based on functional compositions, genes related to multidrug exporters were rich in microbial genomes, whereas genes involved in nutrient importers were rich in microbial transcriptomes. In addition, genes encoding chemotaxis-associated components and glycoside hydrolases specific for plant beta-glycosidic linkages were abundant in both DNA and RNA. This exploratory study provides findings which may help to form molecular-based hypotheses regarding functional contributions of symbiotic gut microbiota in small herbivores with folivorous dietary habits.
Highlights
Mammals and their gut microbiota have co-evolved for millions of years, forming an interdependent, symbiotic relationship (Stevens and Hume, 1998; Ley et al, 2008; Leser and Molbak, 2009)
The pH of feed contents differed among gut chambers (Figure 1D), with stomach contents having a relatively low pH (4-5), small intestine contents being slightly alkaline, and contents in the cecum and large intestine being mildly acidic
In combination with metabolomic data, we identified KEGG pathways with high coverage of KEGG Orthology (KO) and relevant compounds, including pathways involved in substrate-induced cell motility and pathways for biosynthesis of cellular components from plant-sourced nutrients
Summary
Mammals and their gut microbiota have co-evolved for millions of years, forming an interdependent, symbiotic relationship (Stevens and Hume, 1998; Ley et al, 2008; Leser and Molbak, 2009). Small mammalian herbivores usually have a well-developed cecum with a capacity ∼10 times that of their stomach (Manning et al, 1994; Campbell et al, 2000) Their gut structure apparently has a special sorting mechanism at the ileal-cecal-colic junction, permitting fluid and fine particles (including microbes and fine plant debris) to be retained in the cecum, while concurrently allowing coarse dry matter to rapidly pass through the gut (Hume, 2002). Such digestive strategies are believed to satisfy energy demands of small mammalian herbivores with high mass-specific metabolic rates (Sakaguchi, 2003). In contrast to numerous studies on ruminants and ruminal microbiota (Brulc et al, 2009; Weimer, 2015; Mao et al, 2016; Deusch et al, 2017), much less is known about co-adaptation characteristics between small mammalian herbivores and their cecal microbiota
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