Phylogenetic signal in gut microbial community rather than in rodent metabolic traits

Xue-Ying Zhang; Saeid Khakisahneh; Wei Liu; Xinyi Zhang; Weiwei Zhai; Jilong Cheng; John R Speakman; De-Hua Wang

doi:10.1093/nsr/nwad209

Phylogenetic signal in gut microbial community rather than in rodent metabolic traits

Natl Sci Rev. 2023 Jul 28;10(10):nwad209. doi: 10.1093/nsr/nwad209. eCollection 2023 Oct.

Authors

Xue-Ying Zhang¹, Saeid Khakisahneh¹, Wei Liu¹, Xinyi Zhang^{2

3}, Weiwei Zhai^{2

3}, Jilong Cheng², John R Speakman^{4

5

6}, De-Hua Wang^{1

7

8}

Affiliations

¹ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
² Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
³ CAS Center for Excellence in Animal Evolution and Genetics, University of Chinese Academy of Sciences, Kunming 650223, China.
⁴ Shenzhen Key Laboratory of Metabolic Health, Center for Energy Metabolism and Reproduction, Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China.
⁵ Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB39 2PN, UK.
⁶ State Key Laboratory of Molecular Developmental Biology, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.
⁷ School of Life Sciences, Shandong University, Qingdao 266237, China.
⁸ CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China.

Abstract

Host phylogeny and environment have all been implicated in shaping the gut microbiota and host metabolic traits of mammals. However, few studies have evaluated phylogeny-associated microbial assembly and host metabolic plasticity concurrently, and their relationships on both short-term and evolutionary timescales. We report that the branching order of a gut microbial dendrogram was nearly congruent with phylogenetic relationships of seven rodent species, and this pattern of phylosymbiosis was intact after diverse laboratory manipulations. Laboratory rearing, diet or air temperature (T_a) acclimation induced alterations in gut microbial communities, but could not override host phylogeny in shaping microbial community assembly. A simulative heatwave reduced core microbiota diversity by 26% in these species, and led to an unmatched relationship between the microbiota and host metabolic phenotypes in desert species. Moreover, the similarity of metabolic traits across species at different Tas was not correlated with phylogenetic distance. These data demonstrated that the gut microbial assembly showed strong concordance with host phylogeny and may be shaped by environmental variables, whereas host metabolic traits did not seem to be linked with phylogeny.

Keywords: air temperature (Ta); gut microbiota; host–bacteria interactions; metabolic plasticity; phylogenetic signal.