The plant secondary compound swainsonine reshapes gut microbiota in plateau pikas (Ochotona curzoniae)

Shangang Jia,Haibo Fu,Chuanfa Liu,Xianjiang Tang,Yanming Zhang,Chao Fan,Liangzhi Zhang,Shien Ren

doi:10.1007/s00253-021-11478-6

Abstract

Plants produce various plant secondary compounds (PSCs) to deter the foraging of herbivorous mammals. However, little is known about whether PSCs can reshape gut microbiota and promote gut homeostasis of hosts. Using 16S rDNA sequencing to investigate the effects of PSCs on the gut microbiota of small herbivorous mammals, we studied plateau pikas (Ochotona curzoniae) fed diets containing swainsonine (SW) extracted from Oxytropis ochrocephala. Our results showed that both long- and short-term treatment of a single artificial diet in the laboratory significantly reduced alpha diversity and significantly affected beta diversity, core bacteria abundance, and bacterial functions in pikas. After SW was added to the artificial diet, the alpha diversity significantly increased in the long-term treatment, and core bacteria (e.g., Akkermansiaceae) with altered relative abundances in the two treatments showed no significant difference compared with pikas in the wild. The complexity of the co-occurrence network structure was reduced in the artificial diet, but it increased after SW was added in both treatments. Further, the abundances of bacteria related to altered alanine, aspartate, and glutamate metabolism in the artificial diet were restored in response to SW. SW further decreased the concentration of short-chain fatty acids (SCFAs) in both treatments. Our results suggest that PSCs play a key role in regulating gut microbiota community and intestinal homeostasis, thereby maintaining host health.Key points• Swainsonine improves the intestinal bacterial diversity of plateau pikas.• Swainsonine promotes the recovery of core bacterial abundances in the gut of plateau pikas.• Swainsonine promotes the restoration of intestinal bacterial functions of plateau pikas.

Highlights

Over the last few decades, the livestock industry of the Qinghai–Tibet Plateau has developed rapidly, which has rendered 60% of the grassland vulnerable to degradation
Our previous study showed that swainsonine (SW), a toxic indolizidine alkaloid found in plants, promotes resilience and maintains diverse enterotypes in small herbivorous mammals (Fan et al 2020)
We identified the clustering of sequences with 97% similarity into 11,740 operational taxonomic units (OTUs), and 8696 and 8160 OTUs were identified for the long-term and short-term treatments, respectively

Summary

Introduction

Over the last few decades, the livestock industry of the Qinghai–Tibet Plateau has developed rapidly, which has rendered 60% of the grassland vulnerable to degradation. Grasslands dominated by poisonous plants are favored by small herbivorous mammals, which lead to population outbreaks (Smith et al 2019). The outbreak mechanism of small mammal populations caused by grassland degradation and the role of toxic plants in promoting their survival and reproduction has not been well explicated. Our previous study showed that swainsonine (SW), a toxic indolizidine alkaloid found in plants, promotes resilience and maintains diverse enterotypes in small herbivorous mammals (Fan et al 2020). There are many differences between natural and artificial diets in terms of nutrients, trace elements, and PSCs. further studies are required to explore the effect of PSCs on the gut microbiota, illustrating the mutualism mechanism between plants and animals

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