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

Abstract

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.

Impacts of Sediment Particle Grain Size and Mercury Speciation on Mercury Bioavailability Potential

“…Field − and laboratory − studies have demonstrated the existence of biomethylation potentials of nano-HgS in environmental systems. The amount, surface structure, and size distribution of nanophase HgS can affect the transport, reactivity, and methylation potential of Hg in the environment.…”

Diffusion of H2S from anaerobic thiolated ligand biodegradation rapidly generates bioavailable mercury

“…Several studies have shown the central role of sulfide in Hg methylation (Graham et al ., 2012, 2013; Zhou et al ., 2017; Mazrui et al ., 2018; Thomas et al ., 2018; An et al ., 2019; Thomas et al ., 2019; Zhang et al ., 2020; Tian et al ., 2021). Most recently, Tian et al .…”

“…Several studies have shown the central role of sulfide in Hg methylation (Graham et al, 2012(Graham et al, , 2013Zhou et al, 2017;Mazrui et al, 2018;Thomas et al, 2018;An et al, 2019;Thomas et al, 2019;Zhang et al, 2020;Tian et al, 2021). Most recently, Tian et al (2021) described the importance of Hg(II)-sulfides as a major driver of MeHg production.…”

“…Newly formed small Hg(II)–sulfides can permeate readily through cytoplasmic membranes (Zhou et al ., 2017; Thomas et al ., 2018; An et al ., 2019; Thomas et al ., 2019; Tian et al ., 2021). However, given enough time and elevated Hg(II) concentrations, these HgS particles can aggregate and become too large and unavailable to cells (Graham et al ., 2012, 2013; Mazrui et al ., 2018; Zhang et al ., 2020; Tian et al ., 2021).…”

Natural organic matter facilitates formation and microbial methylation of mercury selenide nanoparticles

“…As a matter of fact, precipitation of inorganic divalent mercury and sulfide in the presence of natural organic matter (NOM) led to the formation of nanoparticulate mercury sulfide (HgS, i.e., metacinnabar) that was available for microbial methylation. [15][16][17] Considering that soil microorganisms can reduce selenate and selenite, i.e. the main components of Se-fertilizers, to selenide, [18][19][20][21] co-precipitation of mercuric mercury, selenide and NOM may represent as a potential pathway for forming bioavailable mercury species, particularly nano-HgSe, for MeHg production that induces severe ecological and health risks.…”