Microbial mercury (Hg) methylation transforms a toxic trace metal into the highly bioaccumulated neurotoxin methylmercury (MeHg). The lack of a genetic marker for microbial MeHg production has prevented a clear understanding of Hg-methylating organism distribution in nature. Recently, a specific gene cluster (hgcAB) was linked to Hg methylation in two bacteria.1 Here we test if the presence of hgcAB orthologues is a reliable predictor of Hg methylation capability in microorganisms, a necessary confirmation for the development of molecular probes for Hg-methylation in nature. Although hgcAB orthologues are rare among all available microbial genomes, organisms are much more phylogenetically and environmentally diverse than previously thought. By directly measuring MeHg production in several bacterial and archaeal strains encoding hgcAB, we confirmed that possessing hgcAB predicts Hg methylation capability. For the first time, we demonstrated Hg methylation in a number of species other than sulfate- (SRB) and iron- (FeRB) reducing bacteria, including methanogens, and syntrophic, acetogenic, and fermentative Firmicutes. Several of these species occupy novel environmental niches for Hg methylation, including methanogenic habitats such as rice paddies, the animal gut, and extremes of pH and salinity. Identification of these organisms as Hg methylators now links methylation to discrete gene markers in microbial communities.
. We tested the hypothesis that differences in Hg(II) i sorption and/or uptake rates drive observed differences in methylation rates among Desulfovibrio species. Hg(II) i associated rapidly and with high affinity to both methylating and nonmethylating species. MeHg production by Hg-methylating strains was rapid, plateauing after ϳ3 h. All MeHg produced was rapidly exported. We also tested the idea that all Desulfovibrio species are capable of Hg(II) i methylation but that rapid demethylation masks its production, but we found this was not the case. Therefore, the underlying reason why MeHg production capability is not universal in the Desulfovibrio is not differences in Hg affinity for cells nor differences in the ability of strains to degrade MeHg. However, Hg methylation rates varied substantially between Hg-methylating Desulfovibrio species even in these controlled experiments and after normalization to cell density. Thus, biological differences may drive crossspecies differences in Hg methylation rates. As part of this study, Microbial mercury methylation is the main driver of risk associated with Hg pollution. Methylmercury production is an anaerobic process that occurs in saturated soils and wetlands (26,44,45,53), decaying periphyton mats (1, 14, 31), aquatic bottom sediments (16,27,33,36), and anaerobic bottom waters (56). Early investigations, prior to the advent of modern methylmercury (MeHg) analyses, reported a wide variety of aerobic and anaerobic Gram-positive and Gram-negative bacteria (30,49,55,58) and fungi (55) to be capable of MeHg production. However, subsequent studies with pure cultures have conclusively demonstrated a role only for sulfate-reducing bacteria (SRB) (4,8,11,13,20,23,38,50) and iron-reducing bacteria (FeRB; principally Geobacter spp.) (21, 37), all belonging to the Deltaproteobacteria. Many field studies, using selective microbial stimulants (1, 10, 26, 44, 57), inhibitors (1, 16, 24, 26, 59), and biogeochemical correlates (6,39,40,45), have buttressed the paradigm of SRB and FeRB as the dominant Hg methylators in natural aquatic systems (16,24,59), though recent studies have hypothesized that methanogens may be significant in some systems (31).Only a subset of SRB and FeRB are capable of Hg methylation (11,23,37,50), but why this is the case remains unclear. Early work by Choi and Bartha (13) suggested that Hg methylation was a "metabolic mistake" of SRB utilizing the acetyl coenzyme A (acetyl-CoA) pathway for carbon metabolism. Subsequent studies, however, indicated that Hg methylation capability is not restricted to SRB possessing the acetyl-CoA pathway (20). At present, it is not possible to conclusively identify the methyltransferase or methyl donor in SRB (or other Deltaproteobacteria) responsible for in vivo Hg methylation. Hg methylation occurs intracellularly (23), and significant effort has therefore been devoted to elucidating the mechanism(s) of Hg uptake by Hg-methylating bacteria.Passive diffusion of neutral HgS species has been hypothesized to control Hg uptak...
Methylmercury (MeHg) production was compared among nine cultured methanogenic archaea that contain hgcAB, a gene pair that codes for mercury (Hg) methylation. The methanogens tested produced MeHg at inherently different rates, even when normalized to growth rate and Hg availability. Eight of the nine tested were capable of MeHg production greater than that of spent- and uninoculated-medium controls during batch culture growth. Methanococcoides methylutens, an hgcAB+ strain with a fused gene pair, was unable to produce more MeHg than controls. Maximal conversion of Hg to MeHg through a full batch culture growth cycle for each species (except M. methylutens) ranged from 2 to >50% of the added Hg(II) or between 0.2 and 17 pmol of MeHg/mg of protein. Three of the species produced >10% MeHg. The ability to produce MeHg was confirmed in several hgcAB+ methanogens that had not previously been tested (Methanocella paludicola SANAE, Methanocorpusculum bavaricum, Methanofollis liminatans GKZPZ, and Methanosphaerula palustris E1-9c). Maximal methylation was observed at low sulfide concentrations (<100 μM) and in the presence of 0.5 to 5 mM cysteine. For M. hollandica, the addition of up to 5 mM cysteine enhanced MeHg production and cell growth in a concentration-dependent manner. As observed for bacterial Hg methylators, sulfide inhibited MeHg production. An initial evaluation of sulfide and thiol impacts on bioavailability showed methanogens responding to Hg complexation in the same way as do Deltaproteobacteria. The mercury methylation rates of several methanogens rival those of the better-studied Hg-methylating sulfate- and iron-reducing Deltaproteobacteria.
Understanding the ecological processes that regulate the production and fate of methane (CH 4 ) in wetland soils is essential for forecasting wetland CH 4 emissions. Iron reduction is an important carbon mineralization pathway that is capable of suppressing CH 4 production in freshwater wetlands, but our understanding of temperature regulation of iron oxide respiration and the subsequent impacts on CH 4 production is limited. We tested the hypothesis that temperature regulates iron reduction rates indirectly through differential effects on Fe(II) oxidation versus Fe(III) reduction, which ultimately determines the size of the microbially labile, poorly crystalline Fe(III) pool. Our study indicates that rates of iron reduction are more sensitive to changes in temperature than rates of iron oxidation, which creates imbalance in the relative proportion of Fe(II) and Fe(III) in the poorly crystalline soil iron pool as temperatures change. Our results suggest that warmer temperatures can cause the Fe (III) oxide pool to decline, limiting the Fe(III) supply to iron reducers and relieving competition for organic carbon with methanogens.
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