Gut microbiota contribute to cold adaptation in mammals-primates and ungulates

Abstract

Gut microbiota play an influential role in how animals adapt to extreme environments. Two phylogenetically distant mammals, Yunnan snub-nosed monkey and reindeer both adapted to frigid environments. Metagenomic analyses revealed they developed similar cold adaptation strategies in response to food scarcity (enhanced fiber degradation and nitrogen balance maintenance), energy shortages (increased short-chain fatty acid [SCFA] synthesis), and a constant body temperature sustainment (stimulation of non-shivering thermogenesis [NST]). Moreover, they evolved distinct adaptation strategies to cope with different cold ecosystems. Yunnan snub-nosed monkey adapt to high-altitude hypoxia environment through enhancing ability to synthesize lactate and metabolize purine, while reindeer adapt to extreme cold environment through increasing blood flow, strengthening urea cycling, and enriching fat storage associated bacteria. Notably, reindeer microbiota uniquely enriched cholesterol-degrading bacteria, potentially mitigating cardiovascular risks from lipid storage. Our study expands the knowledge of how gut microbiome promotes cold adaptation through shared and specialized mechanisms shaped by different phylogenetic and ecological contexts.

Keywords: Ecology; Evolutionary biology; Genomics; Zoology.

Graphical abstract

Figure 1

Assessment of SGBs quality and gut microbial diversity (A) Estimated completeness and contamination of 2,771 genomes identified from two cold-adapted mammals and their relatives. Medium-quality genomes are shown in yellow and high-quality genomes in green. (B) Phylogenetic tree of gut representative SGBs. Inner circle is a phylogenetic tree of 2,771 representative SGBs colored according to GTDB phylum-level taxonomic classifications (see color legend). Concentric circles from the inside to the outside represent the family-level taxonomic classification, and the mean relative abundance of SGBs in the RB, RA, RT, and ED samples. (C) Alpha (α) diversity analyses of SGBs between two cold-adapted mammals and their relatives, data are represented as median±SD. The analyses were conducted using the Wilcoxon rank-sum test based on Shannon diversity indices, with ∗ representing FDR<0.05, ∗∗ representing FDR <0.01, and ∗∗∗ representing FDR <0.001. (D and E) Results from (D) UPGMA trees and (E) PCoA, both of which used the Bray-Curtis distance to calculate the relative abundance of SGBs. The 95% confidence ellipses are shown by circular shadows. RB, Yunnan snub-nosed monkey; RT, reindeer; RA, Tonkin snub-nosed monkey; ED, Père David’s deer.

Figure 2

Taxonomic composition of cold-adapted mammals and relatives from warmer climates (A) Relative abundances of the top 5 phylum in each sample. (B) Relative abundances of the top 10 genera in each sample. (C) The differentially enriched phylum in the Yunnan snub-nosed monkey and reindeer (Wilcoxon rank-sum test, FDR <0.05). (D) Genera demonstrating enrichment in both Yunnan snub-nosed monkey and reindeer (Wilcoxon rank-sum test, FDR <0.05), data are represented as median±SD. In the boxplots, green and pink boxes indicate the abundances observed in the Yunnan snub-nosed monkey and reindeer, respectively, while the gray box indicates the abundances in the Tonkin snub-nosed monkey and Père David’s deer. (E) Bubble chart shows the enrichment of core genera in Yunnan snub-nosed monkey and reindeer samples (Wilcoxon rank-sum test, FDR <0.05). The red font indicates the core genera enriched in both cold-adapted mammals. Colored bands in (D) and (E) represent phylum and family level classification information. RB, Yunnan snub-nosed monkey; RT, reindeer; RA, Tonkin snub-nosed monkey; ED, Père David’s deer.

Figure 3

Enrichment of functional characteristics in the gut microbiota of cold-adapted mammals Significantly enriched metabolism-related pathways (A) and modules (B) in the Yunnan snub-nosed monkey and reindeer (Fisher’s test, FDR <0.05); pathways/modules on the left of the Y-axis (X = 0) indicate significant enrichment in the Yunnan snub-nosed monkey, while those on the right indicate significant enrichment in the reindeer; Circular and triangular bubbles represent convergent and species-specific pathways/modules in two cold-adapted mammals, respectively.

Figure 4

Metabolic reconstruction of SGBs enriched in the gut microbiota of cold-adapted mammals Heatmaps showing counts of genes associated with selected significantly enriched functional modules among high-quality SGBs (completeness >90% and contamination <5%) that are significantly enriched in both the Yunnan snub-nosed monkey (A) and reindeer (B) (Fisher’s test, FDR <0.05). Colored bands represent the phyla and families associated with these SGBs. See also Table S9.