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

Abstract

Summary Methylmercury is a potent neurotoxin that biomagnifies through food webs and which production depends on anaerobic microbial uptake of inorganic mercury (Hg) species. One outstanding knowledge gap in understanding Hg methylation is the nature of bioavailable Hg species. It has become increasingly obvious that Hg bioavailability is spatially diverse and temporally dynamic but current models are mostly built on single thiolated ligand systems, omitting ligand exchanges and interactions, or the inclusion of dissolved gaseous phases. In this study, we used a whole‐cell anaerobic biosensor to determine the role of a mixture of thiolated ligands on Hg bioavailability. Serendipitously, we discovered how the diffusion of trace amounts of exogenous biogenic H2S, originating from anaerobic microbial ligand degradation, can alter Hg speciation – away from H2S production site – to form bioavailable species. Regardless of its origins, H2S stands as a mobile mediator of microbial Hg metabolism, connecting spatially separated microbial communities. At a larger scale, global planetary changes are expected to accelerate the production and mobilization of H2S and Hg, possibly leading to increased production of the potent neurotoxin; this work provides mechanistic insights into the importance of co‐managing biogeochemical cycle disruptions.

Coupling Fluorescent Probes to Characterize S-Containing Compounds in a Sulfate Reducing Bacteria Involved in Hg Methylation

“…8a), indicating that P. hydrargyri BerOc1 can degrade thiols such as cysteine to produce biogenic sulfides. Other strains, affiliated with E. coli and G. sulfurreducens, were also demonstrated to degrade cysteine and produce biogenic sulfides [26][27][28]. The presence of these biogenic sulfides could change the speciation of metals such as Hg in solution to form other Hg(II)-sulfide species.…”

“…The presence of these biogenic sulfides could change the speciation of metals such as Hg in solution to form other Hg(II)-sulfide species. Stenzler et al [27] demonstrated that exogenous biogenic sulfide, originating from anaerobic microbial thiol degradation, can alter Hg speciation; nanomolar levels of sulfides were sufficient to change Hg(II) speciation and form aqueous Hg(II)sulfides [i. e., Hg(HS) 2 and Hg(HS) − ] or facilitate the precipitation of metacinnabar (β-HgS(s)), resulting in an increased microbial Hg methylation.…”

“…Maximal methylation was also observed at sulfide concentrations below 200 µM and 100 µM for Pseudodesulfovibrio mercurii ND132 [25] and three strains of methanogenic archaea [3], respectively. Bacteria produce endogenous sulfides through sulfate-reducing metabolism but also by the degradation of thiol compounds, particularly cysteine (i. e., not limited to dissimilatory sulfate reduction) [24,26,27]. Sulfides can outcompete cysteine for Hg(II) binding, typically by precipitating as HgS nanoparticles [16,28,29].…”