Adaptive expression of phage auxiliary metabolic genes in paddy soils and their contribution toward global carbon sequestration

Habitats with intermittent flooding, such as paddy soils, are crucial reservoirs in the global carbon pool; however, the effect of phage-host interactions on the biogeochemical cycling of carbon in paddy soils remains unclear. Hence, this study applied multiomics and global datasets integrated with validation experiments to investigate phage-host community interactions and the potential of phages to impact carbon sequestration in paddy soils. The results demonstrated that paddy soil phages harbor a diverse and abundant repertoire of auxiliary metabolic genes (AMGs) associated with carbon fixation, comprising 23.7% of the identified AMGs. The successful annotation of protein structures and promoters further suggested an elevated expression potential of these genes within their bacterial hosts. Moreover, environmental stressors, such as heavy metal contamination, cause genetic variation in paddy phages and up-regulate the expression of carbon fixation AMGs, as demonstrated by the significant enrichment of related metabolites (P < 0.05). Notably, the findings indicate that lysogenic phages infecting carbon-fixing hosts increased by 10.7% under heavy metal stress. In addition, in situ isotopic labeling experiments induced by mitomycin-C revealed that by increasing heavy metal concentrations, ¹³CO₂ emissions from the treatment with added lysogenic phage decreased by approximately 17.9%. In contrast, ¹³C-labeled microbial biomass carbon content increased by an average of 35.4% compared to the control. These results suggest that paddy soil phages prominently influence the global carbon cycle, particularly under global change conditions. This research enhances our understanding of phage-host cooperation in driving carbon sequestration in paddy soils amid evolving environmental conditions.