Methylmercury, biomagnifying through food chains, is highly toxic for aquatic life. Its production and degradation are largely driven by microbial transformations; however, diversity and metabolic activity of mercury transformers, resulting in methylmercury concentrations in environments, remain poorly understood. Microbial mats are thick biofilms where oxic and anoxic metabolisms cooccur, providing opportunities to investigate the complexity of the microbial mercury transformations over contrasted redox conditions. Here, we conducted a genome-resolved metagenomic and metatranscriptomic analysis to identify putative activity of mercury reducers, methylators and demethylators in microbial mats strongly contaminated by mercury. Our transcriptomic results revealed the major role of rare microorganisms in mercury cycling. Mercury methylators, mainly related to Desulfobacterota, expressed a large panel of metabolic activities in sulfur, iron, nitrogen, and halogen compound transformations, extending known activities of mercury methylators under suboxic to anoxic conditions. Methylmercury detoxification processes were dissociated in the microbial mats with methylmercury cleavage being carried out by sulfide-oxidizing Thiotrichaceae and Rhodobacteraceae populations, whereas mercury reducers included members of the Verrucomicrobia, Bacteroidetes, Gammaproteobacteria, and different populations of Rhodobacteraceae. However most of the mercury reduction was potentially carried out anaerobically by sulfur- and iron-reducing Desulfuromonadaceae, revising our understanding of mercury transformers ecophysiology.