Taxon-Function Decoupling as an Adaptive Signature of Lake Microbial Metacommunities Under a Chronic Polymetallic Pollution Gradient

Adaptation of microbial communities to anthropogenic stressors can lead to reductions in microbial diversity and disequilibrium of ecosystem services. Such adaptation can change the molecular signatures of communities with differences in taxonomic and functional composition. Understanding the relationship between taxonomic and functional variation remains a critical issue in microbial ecology. Here, we assessed the taxonomic and functional diversity of a lake metacommunity system along a polymetallic pollution gradient caused by 60 years of chronic exposure to acid mine drainage (AMD). Our results highlight three adaptive signatures. First, a signature of taxon—function decoupling was detected in the microbial communities of moderately and highly polluted lakes. Second, parallel shifts in taxonomic composition occurred between polluted and unpolluted lakes. Third, variation in the abundance of functional modules suggested a gradual deterioration of ecosystem services (i.e., photosynthesis) and secondary metabolism in highly polluted lakes. Overall, changes in the abundance of taxa, function, and more importantly the polymetallic resistance genes such as copA, copB, czcA, cadR, cCusA, were correlated with trace metal content (mainly Cadmium) and acidity. Our findings highlight the impact of polymetallic pollution gradient at the lowest trophic levels.