Seasonal freeze-thaw drives arsenic metabolism dynamics in sediments of a cold-region lake: microbial gene and community responses

Seasonal freeze-thaw process critically regulates arsenic (As)-metabolizing microorganisms (AMMs) in lake sediments through redox-nutrient dynamics. However, the current understanding of microbially mediated As transformation and mobilization processes under freeze-thaw dynamics remains poorly constrained. This study systematically investigated the successional patterns and driving mechanisms of As-metabolizing functional genes and microbial community structures of AMMs in lake sediments during the freeze-thaw process. This study focused on Lake Wuliangsuhai-a typical mid-high latitude lake in northern China-and employed an integrated framework of co-occurrence networks, Mantel tests, and correlation heatmaps. The results revealed that freeze-thaw processes drive significant AMMs restructuring, altering taxonomic composition and functional gene expression while controlling As environmental fate through regulating microbial metabolic functions, altering redox regimes, and restructuring community interaction networks. Co-occurrence network revealed stage-specific restructuring of microbial interactions during freeze-thaw process: robust mutualism established foundational networks during the pre-freezing stage; simplified modularity reflected functional differentiation during the ice-covered period; post-thaw modularity increased during structural reorganization; and synergistic complexity characterized adaptive strategies during the open-water period. Integrated results from Mantel tests and correlation heatmaps identified total nitrogen (TN), total phosphorus (TP), Fe(II), As(III), and As(V) as key succession drivers, with stage-dependent influences on AMMs. This work elucidates fundamental regulatory mechanisms through which seasonal freeze-thaw processes govern As-metabolizing gene dynamics and microbial ecological functions in lake sediments. It further highlights how microbially driven As transformations exacerbate sedimentary contamination risks under climate change, providing critical theoretical foundations for regional water management and pollution mitigation strategies.IMPORTANCESeasonal freeze-thaw processes in cold lakes dramatically control arsenic pollution risks, but how microbes drive this process remains a critical knowledge gap. This study reveals how winter ice cover and spring thaw create "hot moments" for toxic arsenic release by activating specialized sediment microbes, necessitating stage-specific water quality management. Crucially, nutrient loading (total nitrogen/total phosphorus) exacerbates arsenic (As) transformations by stimulating functional gene expression and microbial interactions. As climate change shortens ice seasons, these contamination pulses may become more frequent and severe. By identifying key microbial indicators and high-risk transition periods, our findings empower lake managers to predict arsenic hazards. This science is vital for safeguarding freshwater ecosystems and human health across ice-affected regions worldwide.