Environmental filtering increases with elevation for the assembly of gut microbiota in wild pikas.

Huan Li,Rui Zhou,Jiapeng Qu,Xiaodan Huang,Jianxiao Zhu

doi:10.1111/1751-7915.13450

Abstract

SummaryDespite their important roles in host nutrition, metabolism and adaptability, the knowledge on how the mammalian gut microbial community assemble is relatively scanty, especially regarding the ecological mechanisms that govern microbiota along environmental gradients. To address this, we surveyed the diversity, function and ecological processes of gut microbiota in the wild plateau pika, Ochotona curzoniae, along the elevational gradient from 3106 to 4331 m on ‘the Roof of the World’—Qinghai‐Tibet Plateau. The results indicated that the alpha, beta and functional diversity of gut microbiota significantly increased with elevation, and elevation significantly explained the variations in the gut microbial communities, even after controlling for geographical distance, host sex and body weight. Some gene functions (e.g. nitrogen metabolism and protein kinases) associated with metabolism were enriched in the high‐altitude pikas. Null model and phylogenetic analysis suggest that the relative contributions of environmental filtering responsible for local gut communities increased with elevation. In addition, deterministic processes dominated gut microbial communities in the high‐altitude (more than 3694 m) pikas, while the percentages of stochastic and deterministic processes were very close in the low‐altitude (3106 and 3580 m) pikas. The observed mechanisms that influence pika gut microbiota assembly and function seemed to be mainly mediated by the internal gut environment and by the external environmental pressure (i.e. lower temperature) in the harsh high‐altitude environment. These findings enhance our understanding of gut microbiota assembly patterns and function in wild mammals from extreme harsh environments.

Highlights

The microbes that inhabit on and inside humans and animals have aroused the interests of scientists all over the world, because of their complexity and diversity, and because they possess a lot of important functions on host, including food digestion (Tremaroli and Ba€ckhed, 2012), immunity regulation (Round and Mazmanian, 2009), disease prevention (TlaskalovaHogenova et al, 2011) and physical development (Sommer and Backhed, 2013)
We address five key questions: (i) Which microbial taxa are associated with elevation? (ii) Does elevation predict alpha and beta diversity of pika gut microbiota? (iii) Which gene functions are enriched in high-altitude pikas? (iv) Is the assembly of pika gut microbiota mainly governed by stochastic or deterministic processes? (v) Are the environmental filtering positively correlated with elevation due to the increasing environmental stress in the high-altitude regions? Our results are of significances for studying the gut microbiota assembly and function in wild mammals for extreme high-altitude environments
We found that the relative abundances of Actinobacteria, Verrucomicrobia, Cyanobacteria and Acidobacteria were positively correlated with elevation, while Tenericutes showed a negative association with elevation (Fig. S2)

Summary

Introduction

The microbes that inhabit on and inside humans and animals have aroused the interests of scientists all over the world, because of their complexity and diversity, and because they possess a lot of important functions on host, including food digestion (Tremaroli and Ba€ckhed, 2012), immunity regulation (Round and Mazmanian, 2009), disease prevention (TlaskalovaHogenova et al, 2011) and physical development (Sommer and Backhed, 2013). The application and development of high-throughput sequencing techniques allow us to investigate and describe the composition and diversity of microbial communities with unprecedented depth, whereas the knowledge on how they assemble remains insufficient To address this question, one effective approach is to borrow a conceptual framework from macro-ecology, in which human and animal microbiota may be regarded as ecological communities and their hosts are viewed as ecosystems (Costello et al, 2012; Burns et al, 2015; Yan et al, 2016). Plateau pika plays a key role in alpine ecosystem function, including increasing plant diversity through creating micro-habitats (burrows), providing food resources for carnivorous animals, improving soil structure, permeability and mixing, and promoting the circulation of ecosystem substances (Smith and Foggin, 1999; Li et al, 2013) These unique features make it especially attractive for studying the gut microbial community assembly along environmental gradients.

Results

Discussion

Experimental procedures