Linkages between rumen microbiome, host, and environment in yaks, and their implications for understanding animal production and management

Abstract

Livestock on the Qinghai-Tibetan Plateau is of great importance for the livelihood of the local inhabitants and the ecosystem of the plateau. The natural, harsh environment has shaped the adaptations of local livestock while providing them with requisite eco-services. Over time, unique genes and metabolic mechanisms (nitrogen and energy) have evolved which enabled the yaks to adapt morphologically and physiologically to the Qinghai-Tibetan Plateau. The rumen microbiota has also co-evolved with the host and contributed to the host's adaptation to the environment. Understanding the complex linkages between the rumen microbiota, the host, and the environment is essential to optimizing the rumen function to meet the growing demands for animal products while minimizing the environmental impact of ruminant production. However, little is known about the mechanisms of host-rumen microbiome-environment linkages and how they ultimately benefit the animal in adapting to the environment. In this review, we pieced together the yak's adaptation to the Qinghai-Tibetan Plateau ecosystem by summarizing the natural selection and nutritional features of yaks and integrating the key aspects of its rumen microbiome with the host metabolic efficiency and homeostasis. We found that this homeostasis results in higher feed digestibility, higher rumen microbial protein production, higher short-chain fatty acid (SCFA) concentrations, and lower methane emissions in yaks when compared with other low-altitude ruminants. The rumen microbiome forms a multi-synergistic relationship among the rumen microbiota services, their communities, genes, and enzymes. The rumen microbial proteins and SCFAs act as precursors that directly impact the milk composition or adipose accumulation, improving the milk or meat quality, resulting in a higher protein and fat content in yak milk and a higher percentage of protein and abundant fatty acids in yak meat when compared to dairy cow or cattle. The hierarchical interactions between the climate, forage, rumen microorganisms, and host genes have reshaped the animal's survival and performance. In this review, an integrating and interactive understanding of the host-rumen microbiome environment was established. The understanding of these concepts is valuable for agriculture and our environment. It also contributes to a better understanding of microbial ecology and evolution in anaerobic ecosystems and the host-environment linkages to improve animal production.

Keywords: environmental adaptation; host metabolic regulations; host-rumen microbiome-environment linkages; management implications; rumen microbiome.

Figure 1

Yaks exposed to natural pastures of different qualities.

Figure 2

Box and whisker plots of rumen fermentation profiles comparing yaks and cattle. (A) The in vivo methane emission comparison (n = 7). (B) The in vitro methane production comparison (n = 9); (C) The in vivo comparison of feed digestibility (n = 3); (D) The in vitro comparison of feed digestibility (n = 9); (E) The rumen fermentation VFA profile (in vivo) (Acetate and TVFA: n = 17; propionate, butyrate, and AP ratio: n = 16); (F) The in vitro rumen fermentation VFA profile (n = 6) (see Supplementary Tables 1–5). Values in parentheses indicate the percentage from the statistical analysis comparing yaks with cattle (cattle represent baseline as zero). Wilcoxon Signed Rank test: **p < 0.01; *p < 0.05; ns = not significantly different from zero. TVFA, total volatile fatty acid; DM, dry matter; NDF, neutral detergent fiber; ADF, acid detergent fiber; AP ratio, acetate to propionate molar ratio.

Figure 3

The summarized host gene, rumen microbiota, and the related microbial pathways and hydrogen balance response to the nutritional deprivation in yaks (adapted from Morais and Mizrahi, 2019). (A) The microbial community involved in the hydrolysis of macromolecules and fermentation processes. A “+” in the parentheses refers to higher relative abundance, a “–” in the parentheses refers to lower relative abundance in yaks; (B) Comparison of methanogenesis and volatile fatty acid (VFA) formation pathways between yaks and cattle (adapted from Zhang Z. et al., 2016). The annotation highlighted in red represents enrichment in the yaks and that in blue represents enrichment in cattle rumen microbiota fermentation. (C) Metabolic hydrogen ([2H]) shifting between yak and cattle in vitro inocula fermentation. In (C) (+) or (–) indicate the enrichment or reduction of the parameters in yaks. (D) Host and rumen microbiome interactions on regulating the VFA, microbial protein genesis, and their absorption (adapted from Qiu et al., 2012).

Figure 4

Hierarchical structure of the environment and host-gut microbe interactions.