Skip to main content
Log in

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

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., et al. (2010). QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7, 335–336.

    Article  CAS  Google Scholar 

  • Degnan, P.H., Taga, M.E., and Goodman, A.L. (2014). Vitamin B 12 as a modulator of gut microbial ecology. Cell Metab 20, 769–778.

    Article  CAS  Google Scholar 

  • Delsuc, F., Metcalf, J.L., Wegener Parfrey, L., Song, S.J., González, A., and Knight, R. (2014). Convergence of gut microbiomes in myrmecophagous mammals. Mol Ecol 23, 1301–1317.

    Article  CAS  Google Scholar 

  • Edgar, R.C. (2013). UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10, 996–998.

    Article  CAS  Google Scholar 

  • Edgar, R.C., Haas, B.J., Clemente, J.C., Quince, C., and Knight, R. (2011). UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200.

    Article  CAS  Google Scholar 

  • Fang, H., Kang, J., and Zhang, D. (2017). Microbial production of vitamin B12: a review and future perspectives. Microb Cell Fact 16, 15.

    Article  Google Scholar 

  • Fouts, D.E., Szpakowski, S., Purushe, J., Torralba, M., Waterman, R.C., MacNeil, M.D., Alexander, L.J., and Nelson, K.E. (2012). Next generation sequencing to define prokaryotic and fungal diversity in the bovine rumen. PLoS One 7, e48289.

    Article  CAS  Google Scholar 

  • Guo, W., Mishra, S., Zhao, J., Tang, J., Zeng, B., Kong, F., Ning, R., Li, M., Zhang, H., Zeng, Y., et al. (2018). Metagenomic study suggests that the gut microbiota of the giant panda (Ailuropoda melanoleuca) may not be specialized for fiber fermentation. Front Microbiol 9, 229.

    Article  Google Scholar 

  • Hu, Y., Thapa, A., Fan, H., Ma, T., Wu, Q., Ma, S., Zhang, D., Wang, B., Li, M., Yan, L., et al. (2020). Genomic evidence for two phylogenetic species and long-term population bottlenecks in red pandas. Sci Adv 6, eaax5751.

    Article  CAS  Google Scholar 

  • Hu, Y., Wu, Q., Ma, S., Ma, T., Shan, L., Wang, X., Nie, Y., Ning, Z., Yan, L., Xiu, Y., et al. (2017). Comparative genomics reveals convergent evolution between the bamboo-eating giant and red pandas. Proc Natl Acad Sci USA 114, 1081–1086.

    Article  CAS  Google Scholar 

  • Ley, R.E., Hamady, M., Lozupone, C., Turnbaugh, P.J., Ramey, R.R., Bircher, J.S., Schlegel, M.L., Tucker, T.A., Schrenzel, M.D., Knight, R., et al. (2008). Evolution of mammals and their gut microbes. Science 320, 1647–1651.

    Article  CAS  Google Scholar 

  • Ley, R.E., Turnbaugh, P.J., Klein, S., and Gordon, J.I. (2006). Human gut microbes associated with obesity. Nature 444, 1022–1023.

    Article  CAS  Google Scholar 

  • Li, J., and Wei, H. (2019). Establishment of an efficient germ-free animal system to support functional microbiome research. Sci China Life Sci 62, 1400–1403.

    Article  Google Scholar 

  • Li, J., Wang, J., and Wei, H. (2020). Strengthening the functional research on the interaction between host genes and microbiota. Sci China Life Sci 63, 929–932.

    Article  CAS  Google Scholar 

  • Li, Y., Guo, W., Han, S., Kong, F., Wang, C., Li, D., Zhang, H., Yang, M., Xu, H., Zeng, B., et al. (2015). The evolution of the gut microbiota in the giant and the red pandas. Sci Rep 5, 10185.

    Article  CAS  Google Scholar 

  • Lozupone, C.A., Stombaugh, J.I., Gordon, J.I., Jansson, J.K., and Knight, R. (2012). Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230.

    Article  CAS  Google Scholar 

  • Maynard, C.L., Elson, C.O., Hatton, R.D., and Weaver, C.T. (2012). Reciprocal interactions of the intestinal microbiota and immune system. Nature 489, 231–241.

    Article  CAS  Google Scholar 

  • Muegge, B.D., Kuczynski, J., Knights, D., Clemente, J.C., González, A., Fontana, L., Henrissat, B., Knight, R., and Gordon, J.I. (2011). Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974.

    Article  CAS  Google Scholar 

  • Qin, N., Dong, X., and Zhao, L. (2018). Microbiome: from community metabolism to host diseases. Sci China Life Sci 61, 741–743.

    Article  Google Scholar 

  • Sommer, F., and Bäckhed, F. (2013). The gut microbiota—masters of host development and physiology. Nat Rev Microbiol 11, 227–238.

    Article  CAS  Google Scholar 

  • Tremaroli, V., and Bäckhed, F. (2012). Functional interactions between the gut microbiota and host metabolism. Nature 489, 242–249.

    Article  CAS  Google Scholar 

  • Wang, Q., Garrity, G.M., Tiedje, J.M., and Cole, J.R. (2007). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73, 5261–5267.

    Article  CAS  Google Scholar 

  • Wei, F., Hu, Y., Zhu, L., Bruford, M.W., Zhan, X., and Zhang, L. (2012). Black and white and read all over: the past, present and future of giant panda genetics. Mol Ecol 21, 5660–5674.

    Article  Google Scholar 

  • Wei, F., Wang, X., and Wu, Q. (2015). The giant panda gut microbiome. Trends MicroBiol 23, 450–452.

    Article  CAS  Google Scholar 

  • Wei, F., Wu, Q., Hu, Y., Huang, G., Nie, Y., and Yan, L. (2019). Conservation metagenomics: a new branch of conservation biology. Sci China Life Sci 62, 168–178.

    Article  CAS  Google Scholar 

  • Wu, Q., Wang, X., Ding, Y., Hu, Y., Nie, Y., Wei, W., Ma, S., Yan, L., Zhu, L., and Wei, F. (2017). Seasonal variation in nutrient utilization shapes gut microbiome structure and function in wild giant pandas. Proc R Soc B 284, 20170955.

    Article  Google Scholar 

  • Xue, Z., Zhang, W., Wang, L., Hou, R., Zhang, M., Fei, L., Zhang, X., Huang, H., Bridgewater, L.C., Jiang, Y., et al. (2015). The bamboo-eating giant panda harbors a carnivore-like gut microbiota, with excessive seasonal variations. mBio 6, e00022–15.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Youngblut, N.D., Reischer, G.H., Walters, W., Schuster, N., Walzer, C., Stalder, G., Ley, R.E., and Farnleitner, A.H. (2019). Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades. Nat Commun 10, 2200.

    Article  Google Scholar 

  • Yu, L., Luan, P.T., Jin, W., Ryder, O.A., Chemnick, L.G., Davis, H.A., and Zhang, Y.P. (2011). Phylogenetic utility of nuclear introns in interfamilial relationships of Caniformia (order Carnivora). Systatic Biol 60, 175–187.

    Article  CAS  Google Scholar 

  • Zhou, W., Nie, Y., Hu, Y., Swaisgood, R.R., Zhang, Y., Liu, D., and Wei, F. (2019). Seasonal and reproductive variation in chemical constituents of scent signals in wild giant pandas. Sci China Life Sci 62, 648–660.

    Article  CAS  Google Scholar 

  • Zhu, L., Wu, Q., Dai, J., Zhang, S., and Wei, F. (2011). Evidence of cellulose metabolism by the giant panda gut microbiome. Proc Natl Acad Sci USA 108, 17714–17719.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fuwen Wei.

Ethics declarations

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

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, G., Wang, X., Hu, Y. et al. Diet drives convergent evolution of gut microbiomes in bamboo-eating species. Sci. China Life Sci. 64, 88–95 (2021). https://doi.org/10.1007/s11427-020-1750-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-020-1750-7

Keywords

Navigation