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SCIENCE CHINA Life Sciences, https://doi.org/10.1007/s11427-020-1750-7

Diet drives convergent evolution of gut microbiomes in bamboo-eating species

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  • ReceivedMar 18, 2020
  • AcceptedMay 21, 2020
  • PublishedJun 29, 2020

Abstract

Gut microbiota plays a critical role in host physiology and health. The coevolution between the host and its gut microbes facilitates animal adaptation to its specific ecological niche. Multiple factors such as host diet and phylogeny modulate the structure and function of gut microbiota. However, the relative contribution of each factor in shaping the structure of gut microbiota remains unclear. The giant (Ailuropoda melanoleuca) and red (Ailurus styani) pandas belong to different families of order Carnivora. They have evolved as obligate bamboo-feeders and can be used as a model system for studying the gut microbiome convergent evolution. Here, we compare the structure and function of gut microbiota of the two pandas with their carnivorous relatives using 16S rRNA and metagenome sequencing. We found that both panda species share more similarities in their gut microbiota structure with each other than each species shares with its carnivorous relatives. This indicates that the specialized herbivorous diet rather than host phylogeny is the dominant driver of gut microbiome convergence within Arctoidea. Metagenomic analysis revealed that the symbiotic gut microbiota of both pandas possesses a high level of starch and sucrose metabolism and vitamin B12 biosynthesis. These findings suggest a diet-driven convergence of gut microbiomes and provide new insight into host-microbiota coevolution of these endangered species.


Funded by

grants from the Strategic Priority Research Program of the Chinese Academy of Sciences(XDB31000000)

the National Natural Science Foundation of China(31821001,31471992,31970386)

the project of Strategic Biological Resources Service Network of the Chinese Academy of Sciences(ZSSD-003)

Foping Nature Reserve

and Fengtongzhai Nature Reserve for their assistances with sample collection.


Acknowledgment

This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31000000), the National Natural Science Foundation of China (31821001, 31471992, 31970386) and the project of Strategic Biological Resources Service Network of the Chinese Academy of Sciences (ZSSD-003). We thank Yang Zhisong, Foping Nature Reserve, and Fengtongzhai Nature Reserve for their assistances with sample collection.


Interest statement

The author(s) declare that they have no conflict of interest.


Supplement

SUPPORTING INFORMATION

The supporting information is available online at https://doi.org/10.1007/s11427-020-1750-7. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.


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  • Figure 1

    Composition and diversity of gut microbiota of the giant and red pandas. A, Phylum-level gut microbiota composition of the wild giant panda (GPW), the captive giant panda (GPC), the wild red panda (RPW), the captive red panda (RPC), the black bear (BB), the common ferret (FE), the polar bear (PB), and the cow (BV). B, Observed OTU number among gut microbiomes of different species. The numbers of observed OTUs of the cow were significantly higher than those of the other five groups (P<0.01) and those of giant pandas were significantly lower than those of BBs (P<0.05). C, Shannon diversity among gut microbiomes of different species. The cow Shannon diversity index was significantly higher than those of the other five groups (P<0.01). ***P<0.01; **P<0.05.

  • Figure 2

    Convergence of gut microbiome structure of the giant and red pandas. A, Left: Hierarchical clustering analysis of gut microbiome structure at the OTU level. The tree was constructed using the unweighted pair group method with arithmetic mean (UPGMA) based on Bray-Curtis distances; right: Host phylogenetic tree constructed using the Timetree tools on http://www.timetree.org. MYA, million years ago. GP, giant panda; RP, red panda; BB, black bear; FE, common ferret; PB, polar bear; BV, cow. B, Principal coordinate analysis (PCoA) of gut microbiome structure at the OTU level using Bray-Curtis distances. The percentage of variation explained by the plotted principal coordinates is indicated on the axes. The circle colors represent herbivorous (green circle), omnivorous (blue circle), carnivorous (red circle), and specialized bamboo (black circle) diets. C, OTUs over-represented for both giant and red pandas, Asiatic black bear, and both the polar bear and common ferret, identified by LEfSe analysis (P<0.05).

  • Figure 3

    Comparative metagenomic analysis of gut microbiome function in the giant and red pandas, the common ferret, and the polar bear. A, KEGG pathway enrichment of gut microbiomes identified by LEfSe analysis in both pandas and their relatives. GP+RP, the giant and red pandas (red box); FE+PB, common ferret, and polar bear (green box). B, The starch and sucrose metabolism pathway was significantly enriched in both pandas. The mean and median relative gene abundances are indicated with solid and dashed lines, respectively. C, Genes (blue circle) involved in vitamin B12 biosynthesis from precorrin 2 in the gut microbiomes of the giant and red pandas. The dotted box indicates the anaerobic pathway.

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