Host specificity and cophylogeny in the "animal-gut bacteria-phage" tripartite system.

Ye Feng, Ruike Wei, Qiuli Chen, Tongyao Shang, Nihong Zhou, Zeyu Wang, Yanping Chen, Gongwen Chen, Guozhi Zhang, Kun Dong, Yihai Zhong, Hongxia Zhao, Fuliang Hu, Huoqing Zheng
Author Information
  1. Ye Feng: Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China. pandafengye@zju.edu.cn.
  2. Ruike Wei: College of Animal Sciences, Zhejiang University, Hangzhou, China.
  3. Qiuli Chen: Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, China.
  4. Tongyao Shang: Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, China.
  5. Nihong Zhou: College of Animal Sciences, Zhejiang University, Hangzhou, China.
  6. Zeyu Wang: Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, China.
  7. Yanping Chen: USDA-ARS Bee Research Laboratory, Beltsville, MD, USA.
  8. Gongwen Chen: College of Animal Sciences, Zhejiang University, Hangzhou, China.
  9. Guozhi Zhang: College of Animal Sciences, Zhejiang University, Hangzhou, China.
  10. Kun Dong: Eastern Bee Research Institute, College of Animal Science and Technology, Yunnan Agricultural University, Kunming, Yunnan, China.
  11. Yihai Zhong: Environment and Plant Protection Institute, Chinese Academy of Tropical Agriculture Sciences, Haikou, Hainan, China.
  12. Hongxia Zhao: Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, China.
  13. Fuliang Hu: College of Animal Sciences, Zhejiang University, Hangzhou, China.
  14. Huoqing Zheng: College of Animal Sciences, Zhejiang University, Hangzhou, China. hqzheng@zju.edu.cn. ORCID

Abstract

Cophylogeny has been identified between gut bacteria and their animal host and is highly relevant to host health, but little research has extended to gut bacteriophages. Here we use bee model to investigate host specificity and cophylogeny in the "animal-gut bacteria-phage" tripartite system. Through metagenomic sequencing upon different bee species, the gut phageome revealed a more variable composition than the gut bacteriome. Nevertheless, the bacteriome and the phageome showed a significant association of their dissimilarity matrices, indicating a reciprocal interaction between the two kinds of communities. Most of the gut phages were host generalist at the viral cluster level but host specialist at the viral OTU level. While the dominant gut bacteria Gilliamella and Snodgrassella exhibited matched phylogeny with bee hosts, most of their phages showed a diminished level of cophylogeny. The evolutionary rates of the bee, the gut bacteria and the gut phages showed a remarkably increasing trend, including synonymous and non-synonymous substitution and gene content variation. For all of the three codiversified tripartite members, however, their genes under positive selection and genes involving gain/loss during evolution simultaneously enriched the functions into metabolism of nutrients, therefore highlighting the tripartite coevolution that results in an enhanced ecological fitness for the whole holobiont.

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MeSH Term

Animals
Host Specificity
Bacteriophages
Gastrointestinal Microbiome
Bees
Bacteria
Phylogeny
Metagenomics
Metagenome

Word Cloud

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