Gut Microbiome Contributes to Cold-climate Adaptation in Lizards

Abstract

ABSTRACTThe metabolic cold-climate adaption hypothesis predicts that animals from cold environments have relatively high metabolic rates compared with their warm-climate counterparts. However, studies testing this hypothesis are sparse. Here, we compared gut microbes between two cold-climate lizard species of the genus Phrynocephalus to test the hypothesis that gut microbiota can help lizards adapt to cold environments by promoting metabolism and absorption efficiency. We kept lizards at 24°C and 30°C for 25 d, and then collected their fecal samples to analyze and compare the microbiota based on 16S rRNA gene sequencing technology. The gut microbiota was mainly composed of Proteobacteria, Firmicutes, Bacteroidetes, and Verrucomicrobia at the phylum level in both species (Proteobacteria > Firmicutes > Verrucomicrobiota in P. erythrurus, and Bacteroidota > Proteobacteria > Firmicutes in P. przewalskii). Further analysis revealed that the gut microbiota contributed to the host’s cold adaptation, but with differences in the relative abundance of these contributory bacteria between the two species. KEGG analysis revealed that the gut microbiota primarily played roles in metabolism, genetic information processing, cellular processes, and environmental information processing in both species. Furthermore, genes related to metabolism were more abundant in P. erythrurus at 24 °C than in other species × temperature combinations, indicating the role of gut microbiota in long-term cold-climate adaptation. Our finding that gut microbiome contributes to cold-climate adaptation in both species but more evidently in P. erythrurus using colder habitats than P. przewalskii throughout a year confirms the gut microbiota’s role in the cold-climate adaptation in lizards.IMPORTANCEThis study proves that temperature affects the composition and relative abundance of the gut microbiota in two Phrynocephalus lizards in a species-specific manner. Both species harbor specific gut microbiota with significant roles in cold-climate adaptation. Specifically, P. erythrurus has a higher Proteobacteria ratio and relative abundance of metabolism-related microbial genes in the gut than P. przewalskii. Given that P. erythrurus uses colder habitats than P. przewalskii throughout a year, these results suggest that gut microbiota contributes to cold-climate adaptation in both species lizards but more evidently in P. erythrurus. This study provides evidence linking gut microbiome with cold adaptation. The co-evolution mechanism between gut microbiota and their hosts in extreme environments will provide new insights into animal adaptation.