Characterisation of the gut microbial community of rhesus macaques in high-altitude environments

Abstract

Background: The mammal intestinal microbiota is involved in various physiological processes and plays a key role in host environment adaption. However, for non-human primates (NHPs), little is known about their gut microbial community in high-altitude environments and even less about their adaption to such habitats. We characterised the gut microbial community of rhesus macaques from multiple high-altitude environments and compared it to those of low-altitude populations. Results: We collected faecal samples of rhesus macaques from four high-altitude populations (above 3000 m) and three low-altitude populations (below 500 m). By calculating the alpha diversity index, we found that high-altitude populations exhibited a higher diversity. Statistical analysis of beta diversity indicated significant differences between high-and low-altitude populations. Significant differences were also detected at the phylum and family levels. At the phylum level, the high-altitude gut microbial community was dominated by Firmicutes (63.42%), while at low altitudes, it was dominated by Bacteroidetes (47.4%). At the family level, the high-altitude population was dominated by Ruminococcaceae (36.2%), while the low-altitude one was dominated by Prevotellaceae (39.6%). Some families, such as Christensenellaceae and Rikenellaceae, were consistently higher abundant in all high-altitude populations. We analysed the overlap of operational taxonomic units (OTUs) in high-altitude populations and determined their core OTUs (shared by all four high-altitude populations). However, when compared with the lowaltitude core OTUs, only 65% were shared, suggesting a divergence in core OTUs. Function prediction indicated a significant difference in gene copy number of 35 level-2 pathways between high-and low-altitude populations; 29 of them were higher in high altitudes, especially in membrane transport and carbohydrate metabolism. Conclusions: The gut microbial community of high-altitude rhesus macaques was significantly distinct from that of low-altitude populations in terms of diversity, composition and function. High-altitude populations were dominated by Firmicutes and Ruminococcace, while in low-altitude populations, Bacteroidetes and Prevotellaceae were dominant. The difference in gut microbiota between these two populations may be caused by differences in host diet, environmental temperature and oxygen pressure. These differentiated gut microbial microorganisms may play a critical role in the adaptive evolution of rhesus macaques to high-altitude environments.

Altitude influences microbial diversity and herbage fermentation in the rumen of yaks

“…In addition, the increase in diversity of human gut microbes also reflects better health and stronger metabolic capacity [ 17 ]. In this study, rumen microbial diversity of yaks increased with altitude, and was comparable to the gastrointestinal tract (GIT) microbial diversity of other mammals, such as pikas [ 11 ] and rhesus macaques [ 18 ]. Therefore, we speculate that the rumen communities of high-altitude yaks may have a higher ability to use high-fiber herbage to help them meet their energy needs in cold and high-altitude habitats.…”

“…In addition to the observed potential probiotics, we found that a potentially pathogenic bacteria, Treponema , also increased with elevation. Some species of Treponema have been detected in the genital and oral tracts of humans [ 40 ], the rumen of yaks [ 41 ], and the gut of rhesus macaques [ 18 ]. They can cause various diseases in these organisms, such as syphilis, yaws, and papillomatous digital dermatitis [ 18 , 42 ].…”

“…Some species of Treponema have been detected in the genital and oral tracts of humans [ 40 ], the rumen of yaks [ 41 ], and the gut of rhesus macaques [ 18 ]. They can cause various diseases in these organisms, such as syphilis, yaws, and papillomatous digital dermatitis [ 18 , 42 ]. Despite the potential risk of these pathogens, their functional roles in yaks still remain unclear and deserve further investigation.…”

Hypoxia: The “Invisible Pusher” of Gut Microbiota

“…SCFA levels in Yak rumens are higher than those in cattle, thus helping them adapt to high altitudes ( Zhang et al, 2016 ). Other animals, such as black-necked cranes ( Grus nigricollis ) ( Wang et al, 2020 ), lizards ( Phrynocephalus vlangalii ) ( Zhang W. et al, 2018 ), Chinese Rhesus macaques ( Macaca mulatta ) ( Zhao et al, 2018 ; Wu et al, 2020b ), Bufo gargarizans ( Xu et al, 2020 ), Tibetan chickens ( Zhou et al, 2016 ) and Tibetan pigs ( Zeng et al, 2020 ), also have high abundances of Ruminococcus in their guts ( Table 1 ). These data indicate the importance of Ruminococcus in plateau adaptation and hypoxia-tolerant animals.…”

Migration effects on the intestinal microbiota of Tibetans

“…Altitude also induces significant differences in their bacterial communities' structure (Lan et al, 2017). The effects of altitude on bacterial alpha diversity and communities' structure has been confirmed in animal experiments (Wu et al, 2020). A skin microbiota study found that human skin microbiota's beta diversity increases with altitude (Li et al, 2019b).…”