Viral insights into the acidification of sulfidic mine tailings

The acidification of sulfidic mine tailings, driven primarily by sulfur- and iron-oxidizing microorganisms, can lead to severe environmental pollution and imperil human health. The role of viruses in this process and its underlying mechanisms yet remain poorly understood. In this study, we recovered 623 species-level viral genomes and 322 prokaryotic genomes from seven metagenomes of mine tailings with pH values ranging from 7.51 to 2.13. We observed that acidification drastically altered geochemical properties and degraded environmental quality, characterized by significant decreases in carbon/nitrogen ratio and heavy metal levels. The structure and function of viral communities were significantly correlated with pH and prokaryotic diversity, showing distinct dynamics across different acidification stages, similar to patterns observed in the prokaryotic community. Notably, potential sulfur-oxidizing prokaryotes increased in relative abundance as pH declined, while their virus-host abundance ratio exhibited a significant positive correlation with pH. Results indicated that viral "top-down" predation on sulfur-oxidizing prokaryotes was likely suppressed during acidification, providing a survival advantage to these organisms over iron-oxidizing counterparts. Moreover, viruses likely reprogrammed the sulfur and iron metabolism of prokaryotic hosts and enhanced their adaptability to environmental stressors through auxiliary metabolic genes. Additionally, a pH- and lifestyle-dependent evolutionary scenario for viruses revealed that frequent recombination and the accumulation of synonymous mutations in lytic viruses and chronic Inoviridae, likely increased their intrapopulation diversity and resilience. These findings provide new insights into the multifaceted roles of viruses in mine tailings acidification, deepening understanding of the underlying mechanisms and advancing potential strategies to mitigate associated environmental risks.