Gut microbiota and their putative metabolic functions in fragmented Bengal tiger population of Nepal

Abstract

Bengal tigers ( Panthera tigris tigris ) serve a pivotal role as an apex predator in forest ecosystems. To increase our knowledge on factors impacting the viability and health of this endangered species, we studied the gut microbiota in 32 individual Bengal tigers from three geographically separated areas (Chitwan National Park (CNP), Bardia National Park (BNP) and Suklaphanta Wildlife Reserve (SWR)) in Nepal, using noninvasive genetic sampling methods. Gut microbiota influence the immune system, impact various physiological functions, and modulates metabolic reactions, that ultimately impact the host health, behavior and development. Across the tiger populations in Nepal, we found significant differences in the composition of microbial communities based on their geographic locations. Specifically, we detected significant differences between CNP and the other two protected areas (CNP vs BNP: pseudo t = 1.944, P = 0.006; CNP vs SWR: pseudo t = 1.9942, P = 0.0071), but no differences between BNP and SWR. This mirrors what has been found for tiger gene flow in the same populations, suggesting gut microbiota composition and host gene flow may be linked. Furthermore, predictive metagenome functional content analysis (PICRUSt) revealed a higher functional enrichment and diversity for significant gut microbiota in the Chitwan tiger population and the lowest enrichment and diversity in Suklaphanta. The CNP tiger population contained higher proportions of microbiota that are associated with predicted functions relevant for metabolism of amino acid, lipid, xenobiotics biodegradation, terpenoides and polyketides than the SWR population. We conclude the tiger population structure, gut microbiota profile and associated functional metabolic categories are correlated, with geographically most separated CNP and SWR tiger population having the most distinct and different host genotype and microbiota profiles. Our work dramatically expands the understanding of tiger microbiota in wild populations and provides a valuable case study on how to investigate genetic diversity at different hierarchical levels, including hosts as well as their microbial communities.

Colonization and Development of the Fecal Microflora of South China Tiger Cubs (<b><i>Panthera tigris amoyensis</i></b>) by Sequencing of the 16S rRNA Gene

“…Previous studies have described the gut and fecal microbiota of the tiger [He et al, 2018a, b, c;Karmacharya et al, 2019]. However, the members of the microbial community of the tiger after birth remain unclear.…”

Developmental stage variation in the gut microbiome of South China tigers

“…These major phyla, Fusobacteria , Firmicutes , Bacteroidetes , Proteobacteria , and Actinobacteriota , which occupied the gut microbiome of SC, were also found in the other two subspecies of tigers, Amur tigers, and Bengal tigers, which are captive in the same zoo as SC is ( Supplementary Tables 3 , 4 ). The same phyla were also reported to occupy the gut microbiome of captive Amur tigers in the northeast of China ( He et al, 2018 ; Ning et al, 2020 ) and Bengal tigers living in Nepal ( Karmacharya et al, 2019 ). Both this study and a study of the gut microbiome of tigers captive in a zoo in Southern China conducted by Jiang et al found that Firmicutes was the major phylum of these three subspecies of tigers ( Jiang et al, 2020 ).…”

The effect of environment on intestinal microbial diversity of Panthera animals may exceed genetic relationship

“…As previously reported, Acidobacteria and Verrucomicrobia were not found in the fecal microbiota of lions ( Mittal et al, 2020 ), tigers ( He et al, 2018 ; Ning et al, 2020 ), and snow leopards ( Zhang et al, 2014 ). Both Acidobacteria and Verrucomicrobia contain enzymes that encode cellulose and hemicellulose and are involved in plant degradation ( Kanokratana et al, 2011 ; Chen et al, 2017 ; Karmacharya et al, 2019 ). We speculate that a certain proportion of Acidobacteria and Verrucomicrobia in Panthera animals’ fecal samples may be related to their prey ( Grieneisen et al, 2019 ; Mittal et al, 2020 ).…”