Temperature seasonality constrains soil T4-like bacteriophage abundance at large spatial scale

Viruses play key roles in regulating soil microbial dynamics and biogeochemical cycles. T4-like bacteriophages, one of the best-studied viral groups, are abundant in soils, but their biogeographical patterns and ecological drivers remain poorly understood. In this study, we performed the first large-scale assessment of soil T4-like bacteriophages based on metagenomic data using viral hallmark genes, revealing broad spatial structure, identifying dominant environmental factors, and projecting shifts under future climate scenarios.

We analyzed two viral hallmark genes, gene 20 (g20) and gene 23 (g23), retrieved from global soil metagenomes, and National Center for Biotechnology Information (NCBI) reference sequences, yielding 2,385 and 2,928 full-length sequences clustered into 1,211 and 1,269 operational taxonomic units (OTUs), respectively. Phylogenetic analysis revealed that only a small fraction of soil-derived sequences could be assigned to established viral families, with most remaining unclassified below the class Caudoviricetes. The relative abundances of g20 and g23 were assessed at 116 sites spanning 14 biomes across six continents. Consistent biogeographic patterns were observed for both genes, with higher relative abundance in tropical climates and lower levels in polar and dry regions, indicating strong climatic influence. Temperature seasonality (BIO4) was identified as the primary environmental driver, showing a significant negative correlation with the relative abundance of both genes. Using an extreme gradient boosting (XGBoost) model, we predicted global distribution patterns based on extrapolation, revealing concordant global trends, with lower relative abundances in regions with greater seasonal temperature variation. Future projections of BIO4 and viral gene abundance further supported this significant negative correlation.

Our findings reveal that temperature seasonality constrains the abundance of soil T4-like bacteriophages, which serve as sensitive indicators of climate-driven environmental shifts and play important ecological roles within soil microbial communities.