Captivity Influences the Gut Microbiome of Rhinopithecus roxellana

Xiaochen Wang; Ziming Wang; Huijuan Pan; Jiwei Qi; Dayong Li; Liye Zhang; Ying Shen; Zuofu Xiang; Ming Li

doi:10.3389/fmicb.2021.763022

Captivity Influences the Gut Microbiome of Rhinopithecus roxellana

Front Microbiol. 2021 Dec 7:12:763022. doi: 10.3389/fmicb.2021.763022. eCollection 2021.

Authors

Xiaochen Wang^{1

2}, Ziming Wang^{1

2}, Huijuan Pan³, Jiwei Qi¹, Dayong Li⁴, Liye Zhang⁵, Ying Shen¹, Zuofu Xiang⁶, Ming Li^{1

7}

Affiliations

¹ CAS Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
² College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China.
³ School of Ecology and Nature Conservation, Beijing Forestry University, Beijing, China.
⁴ Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education), China West Normal University, Nanchong, China.
⁵ Primate Genetics Laboratory, German Primate Center, Leibniz Institute for Primate Research, Göttingen, Germany.
⁶ College of Life Sciences and Technology, Central South University of Forestry and Technology, Changsha, China.
⁷ Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, Kunming, China.

Abstract

Ex situ (captivity in zoos) is regarded as an important form of conservation for endangered animals. Many studies have compared differences in the gut microbiome between captive and wild animals, but few have explained those differences at the functional level due to the limited amount of 16S rRNA data. Here, we compared the gut microbiome of captive and wild Rhinopithecus roxellana, whose high degree of dietary specificity makes it a good subject to observe the effects of the captive environment on their gut microbiome, by performing a metagenome-wide association study (MWAS). The Chao1 index was significantly higher in the captive R. roxellana cohort than in the wild cohort, and the Shannon index of captive R. roxellana was higher than that of the wild cohort but the difference was not significant. A significantly increased ratio of Prevotella/Bacteroides, which revealed an increased ability to digest simple carbohydrates, was found in the captive cohort. A significant decrease in the abundance of Firmicutes and enrichment of genes related to the pentose phosphate pathway were noted in the captive cohort, indicating a decreased ability of captive monkeys to digest fiber. Additionally, genes required for glutamate biosynthesis were also significantly more abundant in the captive cohort than in the wild cohort. These changes in the gut microbiome correspond to changes in the composition of the diet in captive animals, which has more simple carbohydrates and less crude fiber and protein than the diet of the wild animals. In addition, more unique bacteria in captive R. roxellana were involved in antibiotic resistance (Acinetobacter) and diarrhea (Desulfovibrio piger), and in the prevention of diarrhea (Phascolarctobacterium succinatutens) caused by Clostridioides difficile. Accordingly, our data reveal the cause-and-effect relationships between changes in the exact dietary composition and changes in the gut microbiome on both the structural and functional levels by comparing of captive and wild R. roxellana.

Keywords: MWAS; Rhinopithecus roxellana; captive environment; diet composition; gut microbiome.