Marked variations in gut microbial diversity, functions, and disease risk between wild and captive alpine musk deer

Abstract

Maintaining a healthy status is crucial for the successful captive breeding of endangered alpine musk deer (Moschus chrysogaster, AMD), and captive breeding programs are beneficial to the ex-situ conservation and wild population recovery of this species. Meanwhile, the gut microbiota is essential for host health, survival, and environmental adaptation. However, changes in feeding environment and food can affect the composition and function of gut microbiota in musk deer, ultimately impacting their health and adaptation. Therefore, regulating the health status of wild and captive AMD through a non-invasive method that targets gut microbiota is a promising approach. Here, 16S rRNA gene sequencing was employed to reveal the composition and functional variations between wild (N = 23) and captive (N = 25) AMD populations. The results indicated that the gut microbiota of wild AMD exhibited significantly higher alpha diversity (P < 0.001) and greater abundance of the phylum Firmicutes, as well as several dominant genera, including UCG-005, Christensenellaceae R7 group, Monoglobus, Ruminococcus, and Roseburia (P < 0.05), compared to captive AMD. These findings suggest that the wild AMD may possess more effective nutrient absorption and utilization, a more stable intestinal microecology, and better adaption to the complex natural environment. The captive individuals displayed higher metabolic functions with an increased abundance of the phylum Bacteroidetes and certain dominant genera, including Bacteroides, Rikenellaceae RC9 gut group, NK4A214 group, and Alistipes (P < 0.05), which contributed to the metabolic activities of various nutrients. Furthermore, captive AMD showed a higher level of 11 potential opportunistic pathogens and a greater enrichment of disease-related functions compared to wild AMD, indicating that wild musk deer have a lower risk of intestinal diseases and more stable intestinal structure in comparison to captive populations. These findings can serve as a valuable theoretical foundation for promoting the healthy breeding of musk deer and as a guide for evaluating the health of wild-released and reintroduced musk deer in the future. KEY POINTS: • Wild and captive AMD exhibit contrasting gut microbial diversity and certain functions. • With higher diversity, certain bacteria aid wild AMD's adaptation to complex habitats. • Higher potential pathogens and functions increase disease risk in captive AMD.

Keywords: 16S rRNA gene sequencing; Alpine musk deer; Core microbiome; Gut microbial function; Opportunistic pathogens.

Fig. 1

Sampling sites of wild (red triangle) and captive (black triangle) alpine musk deer (AMD)

Fig. 2

Gut microbial community composition in wild and captive AMD. (a) Histogram analysis of the relative abundance of phyla bacteria. (b) Heatmap analysis based on the top 50 genera bacteria. The color scale ranges from blue (low abundance) to red (high abundance). The red, blue, and black characters represent Firmicutes, Bacteroidetes, and other non-dominant phyla bacteria, respectively

Fig. 3

Comparison of gut microbiota diversity and composition between wild and captive AMD. (a) Alpha diversity analysis based on S_obs, Shannon, Chao1, and phylogenetic diversity (PD) indices. (b) Principal coordinates analysis (PCoA) based on the Bray–Curtis distance matrix showing the separation between wild and captive AMD. *P < 0.05 (Wilcoxon rank-sum test), **P < 0.01 and ***P < 0.001

Fig. 4

Difference analysis of dominant bacteria and metabolic function in gut microbiota between wild and captive AMD. Difference analysis of dominant phyla bacteria (a) and dominant genera bacteria (b). Difference analysis of metabolic function based on the KEGG (Kyoto encyclopedia of genes and genomes) database at level 1 (c) and level 2 (d), and EggNOG (evolutionary genealogy of genes: Non-supervised Orthologous Groups) database (e). *P < 0.05 (Wilcoxon rank-sum test), **P < 0.01 and ***P < 0.001. ns, no significant

Fig. 5

Difference analysis of opportunistic pathogens and disease-related function in gut microbiota between wild and captive AMD. (a) Difference analysis of opportunistic pathogens at the phylum level (a) and the genus level (b). (c) Difference analysis of disease-related function based on the KEGG (Kyoto encyclopedia of genes and genomes) database. *P < 0.05 (Wilcoxon rank-sum test), **P < 0.01 and ***P < 0.001. ns, no significant

Fig. 6

Co-occurrence networks of the top 50 bacteria genus in wild and captive AMD. Each line represents Pearson correlation coefficient (|r|≥ 0.5, P < 0.05)