Effects of Extracellular Polymeric Substances on the Formation and Methylation of Mercury Sulfide Nanoparticles.

Growing evidence has suggested that microbial biofilms are potential environmental "hotspots" for the production and accumulation of a bioaccumulative neurotoxin, methylmercury. Here, we demonstrate that extracellular polymeric substances (EPS), the main components of biofilm matrices, significantly interfere with mercury sulfide precipitation and lead to the formation of nanoparticulate metacinnabar available for microbial methylation, a natural process predominantly responsible for the environmental occurrence of methylmercury. EPS derived from mercury methylating bacteria, particularly Desulfovibrio desulfuricans ND132, substantially increase the methylation potential of nanoparticulate mercury. This is likely due to the abundant aromatic biomolecules in EPS that strongly interact with mercury sulfide via inner-sphere complexation and consequently enhance the short-range structural disorder while mitigating the aggregation of nanoparticulate mercury. The EPS-elevated bioavailability of nanoparticulate mercury to D. desulfuricans ND132 is not induced by dissolution of these nanoparticles in aqueous phase, and may be dictated by cell-nanoparticle interfacial reactions. Our discovery is the first step of mechanistically understanding methylmercury production in biofilms. These new mechanistic insights will help incorporate microbial EPS and particulate-phase mercury into mercury methylation models, and may facilitate the assessment of biogeochemical cycling of other nutrient or toxic elements driven by EPS-producing microorganisms that are prevalent in nature.