Coprophagy prevention alters microbiome, metabolism, neurochemistry, and cognitive behavior in a small mammal

Abstract

Many small mammals engage in coprophagy, or the behavior of consuming feces, as a means to meet nutritional requirements when feeding on low-quality foods. In addition to nutritional benefits, coprophagy may also help herbivores retain necessary gut microbial diversity and function, which may have downstream physiological effects, such as maintaining energy balance and cognitive function. Here, we used collars to prevent Brandt’s vole (Lasiopodomys brandtii) from engaging in coprophagy and monitored changes in microbial community structure, energy metabolism, and cognitive performance. In this research, we found that coprophagy prevention decreased alpha diversity of the gut microbiota, and altered proportions of microbial taxa such as Bacteroidetes, Firmicutes, and Oscillospira. Preventing coprophagy resulted in a reduced body mass, and increased food intake. Importantly, coprophagy prevention decreased vole cognitive behavior and altered levels of neurotransmitters in brain. Daily acetate administration was able to reverse some of the coprophagy prevention-induced changes in microbiota composition, metabolism, neurochemistry, and cognitive behavior. These findings identify the functional importance of coprophagy behavior and interactions between the gut microbiota, energy metabolism, and neurological function. Our results suggest that coprophagy contributes to stabilizing the gut microbiota, promoting microbial metabolism, maintaining host energy balance and, consequently, altering cognitive performance.

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Fig. 1: Coprophagy affected the gut microbiota (Experiment 1).
Fig. 2: Coprophagy prevention induces alterations in metabolic phenotypes in voles (Experiment 2).
Fig. 3: Coprophagy prevention induces alterations in cognitive performance and neurodevelopment in voles (Experiment 2).
Fig. 4: Effects of acetate supplementation on host physiology and gut microbiota during coprophagy prevention (Experiment 3).
Fig. 5: Supplementation of acetate can promote the cognitive performance and development of hippocampal neurons during coprophagy prevention (Experiment 3).

Data availability

Raw sequence data are deposited in the NCBI Sequence Read Archive under accession PRJNA588029.

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Acknowledgements

We appreciate the very helpful and constructive comments and suggestions from the three anonymous reviewers and the editor for improving the manuscript. We thank Jianfeng Wang and Bin Chen from Beijing Nebula Medical Laboratory Co., Ltd for helps in 16S rRNA gene sequencing and analyses. We thank all the members of Animal Physiological Ecology Group for their help in the experiments and discussions.

Funding

This research was supported by the National Natural Science Foundation of China (Nos. 31770440 and 31772461), and the Beijing Natural Science Foundation (5172024).

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Conceptualization: X-YZ, T-BB, and D-HW; experiment: T-BB, JW, and S-JT; writing: T-BB, X-YZ, D-HW, and KDK; supervision and project management: D-HW and X-YZ; funding acquisition: D-HW and X-YZ.

Corresponding author

Correspondence to De-Hua Wang.

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Our experimental protocol has been approved by the Ethics Committee of the Institute of Zoology of Chinese Academy of Sciences.

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Bo, T., Zhang, X., Kohl, K.D. et al. Coprophagy prevention alters microbiome, metabolism, neurochemistry, and cognitive behavior in a small mammal. ISME J (2020). https://doi.org/10.1038/s41396-020-0711-6

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