Functional Characteristics of the Flying Squirrel's Cecal Microbiota under a Leaf-Based Diet, Based on Multiple Meta-Omic Profiling

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.

Characterization of faecal and caecal microbiota of free-ranging black-tailed prairie dogs (Cynomys ludovicianus) using high-throughput sequencing of the V4 region of the 16S rRNA gene

“…These authors commented that changes to the metatranscriptome can be identified earlier than changes to the microbial community itself and may be useful as a tool for predicting impending change to the community composition ( Hatton et al , 2017 ). Metatranscriptomic analysis was also cited as an ideal next step in a study characterizing the caecal microbiome of flying squirrels and would be interesting to employ in future studies on the prairie dog microbiome ( Lu et al , 2018 ).…”

Body-size Scaling is Related to Gut Microbial Diversity, Metabolism and Dietary Niche of Arboreal Folivorous Flying Squirrels

“…Bacteroidetes/firmicutes ratio may be related to gut microbiota and host metabolism relationships. Regarding the Bacteroidetes to Firmicutes ratio of gut microbiota, increased Firmicutes was associated with obesity in a laboratory mouse model and humans 55,56,71 ; however, wild animals, especially herbivorous mammals, harbor much more Firmicutes than Bacteroidetes [72][73][74] . For strictly leaf-based diet cases, folivorous mammals can be either foregut-or hindgut-fermenters, with distinct strategies to degrade a high-fiber diet 9 , thereby contributing to unique gut microbial communities.…”

Variation in gut microbial contribution of essential amino acids to host protein metabolism in a wild small mammal community

“…We found clear distinctions in faecal microbial communities, particularly for bacteria, among Dipodomys species (Figures S3–S11; Tables S2 and S3). Recent work has correlated changes in gut microbial diversity and activity to seasonal dietary shifts in wild black howler monkeys ( Alouatta pigra ; Amato et al, 2015) and plateau pika ( Ochotona curzoniae ; Wang et al, 2020), and advances in genomic sequencing and metabolite profiling now allow for direct comparisons between gut microbial community composition, gut microbial activity and host digestive environment (Lu et al, 2018). Our study demonstrates the utility of AA δ 13 C and δ 15 N analysis in connecting host nutrient acquisition to gut microbial activity and provides preliminary evidence of seasonal variation in the proportional contributions of gut microbiota as AA ESS sources in Dipodomys (Figure S14; Table S10).…”