Characterization of the Gut Microbiota in Six Geographical Populations of Chinese Rhesus Macaques (Macaca mulatta), Implying an Adaptation to High-Altitude Environment

Zhao, Junsong; Yao, Yongfang; Li, Diyan; Xu, Huaming; Wu, Jiayun; Wen, Anxiang; Xie, Meng; Ni, Qingyong; Zhang, Mingwang; Peng, Guangneng

doi:10.1007/s00248-018-1146-8

Cited by 98 publications

(112 citation statements)

References 64 publications

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“…In our study, the observed OTU numbers were lower in both the skin and gut microbiomes of amphibians at high altitude (or in Bg alone), similar to the OTU values observed in humans, pigs, and Chinese rhesus macaques at high and low altitudes (Zeng et al, ; Zhao et al, ). The environment can affect symbiotic microbial diversity (skin and gut microbes) in amphibians (Chang et al, ; Wolz, Yarwood, Grant, Fleischer, & Lips, ).…”

Section: Discussionsupporting

confidence: 88%

“…The results of previous studies showed that although plateau pika have a lower dietary diversity (types of food) than Daurian pika, the amount of gut microbes ( Prevotella and Ruminococcus ) was higher in plateau pika, which could improve their ability to digest plants and increase the observed levels of biodegradation (Li et al, ). Taken together, these studies show that an increased abundance of specific gut microorganisms improves the overall digestibility of nutrients in mammals living at high altitude (Li et al, ; Zhang et al, ; Zhao et al, ). The effect of altitude on the gut microbiome has also been investigated in other vertebrates, such as Tibetan chickens (Zhou et al, ) and lizards (Zhang et al, ).…”

Section: Introductionmentioning

confidence: 90%

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Changes in the community structure of the symbiotic microbes of wild amphibians from the eastern edge of the Tibetan Plateau

et al. 2020

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Environment has a potential effect on the animal symbiotic microbiome. Here, to study the potential relationship of the symbiotic microbiomes of wild amphibians with altitude, we collected the gut and skin samples from frogs (nine species) and the environmental samples (water and soil samples) from the Leshan Mountains (altitude: 360–410 m) and Gongga Mountains (altitude: 3340–3989 m) on the eastern edge of the Tibetan Plateau. Bufo gargarizans (Bg) samples were collected from both the Leshan and Gongga mountain regions (Bg was the only species sampled on both mountains). The DNA extracted from each sample was performed high‐throughput sequencing (MiSeq) of bacterial 16S rRNA gene amplicons. High relative abundance of Caulobacteraceae and Sphingomonadaceae was found in skin samples from both Bg and the other high‐altitude amphibians (nine species combined). High relative abundance of Coxiellaceae and Mycoplasmataceae was found in gut samples from both Bg and the other high‐altitude amphibians. Furthermore, the alpha and beta diversities of skin and gut samples from Bg and the other amphibian species (nine species combined) were similar. In terms of the symbiotic microbial community, the low‐altitude samples were less diverse and more similar to each other than the high‐altitude samples were. We speculated that extreme high‐altitude environments and host phylogeny may affect the amphibian microbiome. Despite the distinct microbial community differences between the skin and gut microbiomes, some functions were similar in the Bg and combined high‐altitude samples. The Bg and high‐altitude skin samples had higher oxidative stress tolerance and biofilm formation than the low‐altitude skin samples. However, the opposite results were observed for the Bg and high‐altitude gut samples. Further study is required to determine whether these characteristics favor high‐altitude amphibian adaptation to extreme environments.

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Section: Discussionsupporting

confidence: 88%

Section: Introductionmentioning

confidence: 90%

Changes in the community structure of the symbiotic microbes of wild amphibians from the eastern edge of the Tibetan Plateau

et al. 2020

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“…This food provisioning is likely leads to a high-fat diet, which probably reduce the gut microbial diversity (Jami, White, & Mizrahi, 2014;Ley, Turnbaugh, Klein, & Gordon, 2006;Murphy et al, 2010). To date, there has been much research on the gut microbiota of rhesus macaques, including as laboratory animals for human gut microbiota research (Ardeshir et al, 2014;Martin et al, 2013;O'Sullivan et al, 2013), and the relationship between the gut microbiota and ecology of these monkeys (Cui, Wang, Yu, Ye, & Yang, 2019;Yasuda et al, 2015;Zhao et al, 2018), but the effect of partial food provisioning on the gut microbiota of rhesus macaques has not been investigated. Therefore, this research may provide advice for the management and protection of provisioned macaques.…”

Section: Introductionmentioning

confidence: 99%

Gut microbiota of provisioned and wild rhesus macaques (Macaca mulatta) living in a limestone forest in southwest Guangxi, China

Chen

Liang

et al. 2019

MicrobiologyOpen

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The gut microbiota plays an important role in animal health and is strongly affected by the environment. Captivity and human source food have been shown to influence drastically the gut microbiota composition and function of wild animals. Therefore, in the present study, the gut microbiota of provisioned and wild populations of limestone‐living rhesus macaques (Macaca mulatta) were compared using high‐throughput 16S rRNA sequencing and bioinformatic analyses. The results indicated that provisioned macaques had a higher microbial richness than wild macaques, but there was no significant difference in the evenness of the gut microbiota between the two populations. Provisioned macaques also showed a higher abundance of Firmicutes and a lower abundance of Bacteroidetes than wild macaques. Functional analysis revealed that wild macaques had enriched microbial pathways involved in glycan biosynthesis and metabolism, transport and catabolism, and the digestive and endocrine systems, while provisioned macaques were richer in pathways associated with signaling molecules and interaction, neurodegenerative diseases. These differences were likely due to modification of the gut microbiota of the provisioned macaques to enable the digestion of new foods.

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“…Our previous work based on elevational gradients found that the abundance of Christensenellaceae was significantly higher in Tibet (3,427 m) than in other geographical populations (5, 158, 1,161, 1,629 2,895 m) [44]. However, our study has several limitations, of which the main one is that only one high-altitude site with six samples was included, which may not represent the universal features of the microbiota composition in high-altitude environments.…”

Section: Composition Difference Between High-altitude and Low-altitudmentioning

confidence: 87%

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

Yao

Dong

et al. 2020

Preprint

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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 3,000 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 highaltitude populations and determined their core OTUs (shared by all four high-altitude populations).However, when compared with the low-altitude 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 lowaltitude 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 4 rhesus macaques to high-altitude environments. BackgroundThe gastrointestinal tract of animals is habited by a complex microbial community, known collectively as the gut or intestinal microbiota. There is increasing evidence that the gut microbial community of animals is involved in a wide range of processes in the host, including health, grow and development as well as behaviour; it can even affect the nervous system by secreting metabolites [1][2][3][4][5][6][7][8][9][10][11]. These microbes can also assist in energy uptake and meta...

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Characterization of the Gut Microbiota in Six Geographical Populations of Chinese Rhesus Macaques (Macaca mulatta), Implying an Adaptation to High-Altitude Environment

Cited by 98 publications

References 64 publications

Changes in the community structure of the symbiotic microbes of wild amphibians from the eastern edge of the Tibetan Plateau

Changes in the community structure of the symbiotic microbes of wild amphibians from the eastern edge of the Tibetan Plateau

Gut microbiota of provisioned and wild rhesus macaques (Macaca mulatta) living in a limestone forest in southwest Guangxi, China

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

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