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

Po-Yu Liu,Tatsuo Oshida,An-Chi Cheng,Shiao-Wei Huang,Hon-Tsen Yu,Hsiao-Pei Lu,Wenhua Liu

doi:10.1038/s41598-020-64801-y

Abstract

Thermal homeostasis of mammals is constrained by body-size scaling. Consequently, small mammals require considerable energy to maintain a high mass-specific metabolic rate (MSMR) and sustain target body temperature. In association with gut microbiota, mammalian hosts acquire absorbable molecules and fulfill their metabolic requirements. Our objective was to characterize gut microbes in wild mammals and relate those findings to host body-size scaling. Two large (Petaurista philippensis grandis and P. alborufus lena), one medium (Trogopterus xanthipes) and one small (Pteromys volans orii) species of flying squirrels (FS) were studied. Using 16S rRNA genes, 1,104 OTUs were detected from four FS, with 1.99% of OTUs shared among all FS. Although all FS gut microbiota were dominated by Firmicutes, they were constituted by different bacterial families. Moreover, Bacteroidetes accounted for up to 19% of gut microbiota in small FS, but was absent in large FS. Finally, based on metagenome predictions, carbohydrate and amino acid metabolism genes were enriched in small body-size FS. In conclusion, gut microbiota compositions and predictive metabolic functions were characteristic of body-size in FS, consistent with their adaptations to folivorous dietary niches.

Highlights

Body size is a major factor in endothermic animals’ metabolism to promote survival
We hypothesized that gut microbiota and microbial energy metabolism are constrained by body-size scaling and that gut microbial composition and functions reflect dietary niches of each flying squirrel species
Strictly folivorous mammals may rely on gut microbiota to maintain a mass-specific metabolic rate

Summary

Introduction

Body size is a major factor in endothermic animals’ metabolism to promote survival. Mammals metabolize foods to generate enough heat to balance surface heat loss[1]. Body size and energy metabolism fundamentally constrain the interaction between animals and their environment and determine their niche It remains unclear how small arboreal folivorous mammals maintain a high MSMR as they have small to moderate body sizes (~250 to 8200 g), due to both physical (habitat structures) and energetic (poor diet) limitations of living in treetops[6,7,8]. Hosts acquire fitness within specific dietary niches that are reflected in variation in several dominant microbial taxa, www.nature.com/scientificreports e.g. phyla Firmicutes, Bacteroidetes, Actinobacteria and Proteobacteria[13,17,18,19] With these diversified symbionts, microbes colonizing mammalian gastrointestinal tracts may have adapted distinct functions. We hypothesized that gut microbiota and microbial energy metabolism are constrained by body-size scaling and that gut microbial composition and functions reflect dietary niches of each flying squirrel species. Thereafter, we predicted the metagenome and pathways of energy metabolism contributed by gut microbiota

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Conclusion