Eco-evolutionary dynamics of gut phageome in wild gibbons (Hoolock tianxing) with seasonal diet variations

Shao-Ming Gao, Han-Lan Fei, Qi Li, Li-Ying Lan, Li-Nan Huang () and Peng-Fei Fan ()
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Shao-Ming Gao: Sun Yat-sen University
Han-Lan Fei: Sun Yat-sen University
Qi Li: Sun Yat-sen University
Li-Ying Lan: Sun Yat-sen University
Li-Nan Huang: Sun Yat-sen University
Peng-Fei Fan: Sun Yat-sen University

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract It has been extensively studied that the gut microbiome provides animals flexibility to adapt to food variability. Yet, how gut phageome responds to diet variation of wild animals remains unexplored. Here, we analyze the eco-evolutionary dynamics of gut phageome in six wild gibbons (Hoolock tianxing) by collecting individually-resolved fresh fecal samples and parallel feeding behavior data for 15 consecutive months. Application of complementary viral and microbial metagenomics recovers 39,198 virulent and temperate phage genomes from the feces. Hierarchical cluster analyses show remarkable seasonal diet variations in gibbons. From high-fruit to high-leaf feeding period, the abundances of phage populations are seasonally fluctuated, especially driven by the increased abundance of virulent phages that kill the Lachnospiraceae hosts, and a decreased abundance of temperate phages that piggyback the Bacteroidaceae hosts. Functional profiling reveals an enrichment through horizontal gene transfers of toxin-antitoxin genes on temperate phage genomes in high-leaf season, potentially conferring benefits to their prokaryotic hosts. The phage-host ecological dynamics are driven by the coevolutionary processes which select for tail fiber and DNA primase genes on virulent and temperate phage genomes, respectively. Our results highlight complex phageome-microbiome interactions as a key feature of the gibbon gut microbial ecosystem responding to the seasonal diet.

Date: 2024
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DOI: 10.1038/s41467-024-45663-8

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