Glacial meltwater drives gene-specific diversification of metal resistance genes in High Arctic soil microbiomes

Climate warming accelerates glacial meltwater delivery to Arctic lakes, mobilizing metals from thawing catchments and reshaping the selective landscape experienced by resident microbes. Whether these gradients leave detectable evolutionary signatures in environmental resistance genes remains unclear. We investigated four metal resistance genes (merA, arsC, cadA, and chrR) in metagenomic datasets from Lake Hazen (Nunavut, Canada), the largest High Arctic freshwater lake, sampled across a natural hydrological gradient of Control, Low-runoff, and High-runoff regimes. Using a space-for-time design, we combined population-genetic and codon-based approaches to quantify diversity and selection, including nucleotide diversity, Tajimas D, nonsynonymous/synonymous diversity ratios, McDonald-Kreitman tests, site-level episodic selection, and Bayesian coalescent and structured-coalescent inference of gene-pool diversity and exchange. This multi-pronged approach allowed us to distinguish gene-specific evolutionary responses from broader demographic effects. We found marked heterogeneity among genes: merA showed increasing diversity and consistent evidence of adaptive evolution along the runoff gradient; cadA displayed the strongest adaptive signal under low runoff, with selective constraint patterns that varied across regimes; chrR exhibited the clearest signature of episodic positive selection, with gene-wide selection and adaptive substitutions concentrated in the high-runoff regime where chromium concentrations were greatest; while arsC remained largely consistent with neutral evolution across regimes. Together, these results show that climate-driven metal mobilization is associated with gene- and regime-specific diversification of microbial metal resistance gene pools in Arctic soil microbiomes. Differences in metal speciation (with arsenic and chromium occurring as redox-sensitive oxyanions, and mercury, cadmium and zinc as divalent cations) may contribute to the contrasting evolutionary trajectories observed across genes, although in-situ speciation was not assessed in this dataset. Our findings highlight environmental resistance genes as sensitive indicators of changing biogeochemical conditions in rapidly warming polar ecosystems.