Enhanced mutualistic symbiosis between soil phages and bacteria with elevated chromium-induced environmental stress

Background: Microbe-virus interactions have broad implications on the composition, function, and evolution of microbiomes. Elucidating the effects of environmental stresses on these interactions is critical to identify the ecological function of viral communities and understand microbiome environmental adaptation. Heavy metal-contaminated soils represent a relevant ecosystem to study the interplay between microbes, viruses, and environmental stressors. Results: Metagenomic analysis revealed that Cr pollution adversely altered the abundance, diversity, and composition of viral and bacterial communities. Host-phage linkage based on CRISPR indicated that, in soils with high Cr contamination, the abundance of phages associated with heavy metal-tolerant hosts increased, as did the relative abundance of phages with broad host ranges (identified as host-phage linkages across genera), which would facilitate transfection and broader distribution of heavy metal resistance genes in the bacterial community. Examining variations along the pollutant gradient, enhanced mutualistic phage-bacterium interactions were observed in the face of greater environmental stresses. Specifically, the fractions of lysogens in bacterial communities (identified by integrase genes within bacterial genomes and prophage induction assay by mitomycin-C) were positively correlated with Cr contamination levels. Furthermore, viral genomic analysis demonstrated that lysogenic phages under higher Cr-induced stresses carried more auxiliary metabolic genes regulating microbial heavy metal detoxification. Conclusion: With the intensification of Cr-induced environmental stresses, the composition, replication strategy, and ecological function of the phage community all evolve alongside the bacterial community to adapt to extreme habitats. These result in a transformation of the phage-bacterium interaction from parasitism to mutualism in extreme environments and underscore the influential role of phages in bacterial adaptation to pollution-related stress and in related biogeochemical processes.