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

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.

Seasonal variations in the composition and functional profiles of gut microbiota reflect dietary changes in plateau pikas

“… 2021 ; Ren et al . 2021 )—for example, berberine promoted Akkermansia growth via stimulating mucin secretion in colon of mice (Dong et al . 2021 ).…”

“… 2014 ; Ren et al . 2021 ). These weeds have high contents of secondary compounds, explaining why the relative abundance of Verrucomicrobiota and Akkermansiaceae in summer was much higher than that in other seasons…”

“…In contrast to the gut microbiota of other plateau mammals such as the Tibetan wild ass (Equus kiang) (Gao et al 2020) and yak (Gong et al 2020), the abundance of Verrucomicrobiota in the intestines of the plateau pikas was very high, and had the highest relative abundance in summer. Akkermansia, the dominant resident genus of phylum Verrucomicrobiota, is well characterized to be an obligate host mucin degrader and usually be promoted by plant secondary compounds in food (Zhang et al 2018b;Dong et al 2021;Ren et al 2021)-for example, berberine promoted Akkermansia growth via stimulating mucin secretion in colon of mice (Dong et al 2021). In July, the diet of plateau pikas contains poisonous weeds, such as Oxytropis ochrocephala, which are often more abundant and are not eaten by livestock (Lu et al 2014;Ren et al 2021).…”

“…Akkermansia, the dominant resident genus of phylum Verrucomicrobiota, is well characterized to be an obligate host mucin degrader and usually be promoted by plant secondary compounds in food (Zhang et al 2018b;Dong et al 2021;Ren et al 2021)-for example, berberine promoted Akkermansia growth via stimulating mucin secretion in colon of mice (Dong et al 2021). In July, the diet of plateau pikas contains poisonous weeds, such as Oxytropis ochrocephala, which are often more abundant and are not eaten by livestock (Lu et al 2014;Ren et al 2021). These weeds have high contents of secondary compounds, explaining why the relative abundance of Verrucomicrobiota and Akkermansiaceae in summer was much higher than that in other seasons Our results showed that the simplest co-occurrence network of the plateau pikas' gut microbiota was in winter (Fig.…”

Anthropogenic disturbance promotes the diversification of antibiotic resistance genes and virulence factors in the gut of plateau pikas (Ochotona curzoniae)

“…Recent studies on gut microbes have shown that gut microbes provide physiological functions to the host, especially herbivores (Kohl et al, 2014(Kohl et al, , 2018. Most of the research on the plateau pika gut microbiome has focused on altitude, plant secondary compounds, and seasonal dynamics (Li et al, 2018(Li et al, , 2019Fan et al, 2020Fan et al, , 2022Ren et al, 2021;Yu et al, 2022). Few reports exist on the effects of resistance genes and virulence factors on intestinal flora composition and function, and whether these effects are exacerbated by pollution from anthropogenic activities.…”