Research highlights: elucidation of biogeochemical factors influencing methylmercury production

Abstract

Coal combustion and other human activities release inorganic mercury into the atmosphere at levels far greater than emissions from natural sources, significantly perturbing the global mercury cycle. Subsequent biogeochemical transformation of inorganic mercury to highly toxic methylmercury allows this heavy metal pollutant to enter the food web, where it bioaccumulates and can have severe impacts on animal and human populations. This Highlight features recent articles that examine in detail the effects of nutrient availability on the methylation–demethylation activity of microorganisms living in sediment with mercury contamination. By investigating differences in levels of sulfate, iron, organic matter, and other environmental factors, this research provides insight into the conditions that may favor methylmercury formation and thereby better inform remediation efforts in the future.

Introduction

Mercury (Hg), a heavy metal element, is widely recognized as an environmental pollutant with direct impact on human populations. Although there exists a natural background level of mobile Hg, anthropogenic emissions from combustion of fossil fuels such as coal have increased the load by a factor of three to five and have dramatically affected the mercury cycle (Fig. 1) (Selin, Ann. Rev. Environ. Resour., 2009, 34, 43). Hg released into the atmosphere by human activity is eventually deposited into aquatic and terrestrial compartments. It is here where inorganic Hg is transformed with varying efficiency to methylmercury (MeHg), which may subsequently be taken up by organisms living in close contact with soils and sediments. Hg is methylated mainly by sulfate and iron reducing bacteria, and to a lesser extent methanogens, found in the anoxic zone of soils and sediments (Selin, Ann. Rev. Environ. Resour., 2009, 34, 43). MeHg is rapidly bioaccumulated and biomagnified in aquatic systems, and consequently the consumption of fresh and saltwater fish represents the primary MeHg exposure route for humans (Driscoll et al., Environ. Sci. Technol., 2013, 47, 4967). MeHg is a potent neurotoxin, and is also known to cause reproductive and immunological harm to a variety of vertebrates (Boening, Chemosphere, 2000, 40, 1335).

Fig. 1 Selected pathways for the biogeochemical transformation of Hg. Hg is released by coal combustion as Hg⁰, Hg²⁺, and particulate-bound mercury Hg(P). Atmospheric oxidation of volatile Hg⁰ produces Hg²⁺, a more water-soluble species that can readily enter aquatic and terrestrial systems. Methylation of inorganic Hg by sulfate reducing bacteria generates toxic MeHg that can be taken up by organisms such as plankton, crustaceans, and fish.

Due to the risks posed by MeHg to human and environmental health, much research has been done on the biogeochemical cycling of Hg and the resulting formation of MeHg. The recent publications highlighted in this article are excellent examples of the work that continues to provide valuable new insights into the biogeochemistry affecting the formation and transport of MeHg. The research done by these authors and others in the field allow policymakers to better assess regulatory and remediation measures to reduce human and wildlife exposure to MeHg.

Mineral inputs impacting methylation–demethylation dynamics

In areas with varying exposure to nutrients such as sulfate, iron, and organic matter, differences in the existing microbial community can lead to differing rates of Hg methylation and demethylation. As bacterial communities are primarily responsible for the net formation or loss of MeHg in a particular location, elucidation of factors that influence their activity is essential to understanding the cycling of Hg in specific environments. Bravo et al. illustrate this point in a recent publication, where the in situ Hg methylation was compared in subsurface sediments at two different locations in Vidy Bay of Lake Geneva, Switzerland (Bravo et al., Water Res., 2015, 80, 245). The two sampling sites were located at either 190 m (site CP) or 530 m (site FP) from the discharge pipe of a sewage treatment plant. Bravo et al. found that while both sites contained similar amounts of total Hg, site CP had a considerably higher amount in the form of MeHg (Fig. 2). Site CP had much higher concentrations of organic matter as well as total iron, due to the residual hydrated ferric oxide used to remove phosphorus in the sewage treatment plant.

Fig. 2 Concentration profiles at each site for (a and b) dissolved Fe²⁺ and solid Fe³⁺, (c and d) solid S/Fe ratios and organic matter (OM) content (%), and (e and f) % MeHg to total concentration of Hg. Reproduced (adapted) with permission from A. G. Bravo, S. Bouchet, S. Guédron, D. Amouroux, J. Dominik and J. Zopfi, Water Res., 2015, 80, 245–255.

To study the Hg methylation–demethylation dynamics at these sites, stable Hg isotope incubation studies were performed on sediments from each site. Sediment from each of the sites was incubated with ¹⁹⁹Hg²⁺ and Me²⁰¹Hg simultaneously. By following the speciation of the individual Hg isotopes with time, the rates of both MeHg formation and consumption can be determined. Apart from the overall Hg concentration, the ratio of these two processes is vitally important to the observed level of MeHg contamination at a given location. Sediment incubation studies suggested that the higher MeHg % seen at site CP is a result of low rates of MeHg demethylation. Geochemical and microbiological analysis showed that iron reduction dominated at site CP, while sulfate reduction dominated at FP. Based on these data, Bravo et al. conclude the suppression of sulfate reducing bacteria coupled with the promotion of iron reducing bacteria and other possible microbes leads to higher net Hg methylation at the sewage treatment plant impacted site.

Mobilization of Hg from permafrost

Long-range atmospheric transport has deposited Hg in soils and sediments worldwide. Much of the Hg contained in soils becomes immobilized for extended periods of time. In some environments, this stored Hg pool may begin to cycle again once disturbed. One such environment exists in the Arctic, where Hg may be mobilized and methylated in permafrost thaw ponds. In a recent publication, MacMillan et al., investigate the potential of these thaw ponds to act as MeHg sources in the warming Canadian Arctic (MacMillan et al., Environ. Sci. Technol., 2015, 49, 7743). Permafrost thaw ponds are small, shallow ponds created by melting snow and permafrost, and represent a major aquatic ecosystem in the Arctic (Vincent & Laybourn-Parry, Polar Lakes and Rivers: Limnology of Arctic and Antarctic Aquatic Ecosystems, 2008, DOI: 10.1093/acprof:oso/9780199213887.003.0002). Upon permafrost melting, these ponds can receive high inputs of organic carbon and other nutrients, making them potential hotspots for Hg methylation. In their publication, MacMillan et al. sampled water from a number of thaw ponds and lakes in two locations in Arctic and sub-Arctic Canada for total Hg, MeHg, organic carbon, and a host of other relevant parameters. Their results showed that thaw pond waters contained on average 24 times the concentration of total Hg contained in lakes. Furthermore, thaw ponds contained significantly higher % MeHg values than the lakes. The high Hg and MeHg found in these thaw ponds is likely due to a combination of high organic matter input when compared to lakes, and anoxic, reducing sediment conditions which aid in the dissolution of Hg mineral phases, making it more bioavailable. All of this creates favorable conditions for the microbial methylation of Hg. The data showed a significant correlation between MeHg concentrations and nutrient inputs such as dissolved organic carbon and total nitrogen (Fig. 3). CO₂ and CH₄, both markers for microbial activity, also correlated significantly with MeHg concentrations. Interestingly, no correlation was observed between SO₄²⁻ and MeHg, suggesting that, as was observed by Bravo et al., sulfate reducing bacteria were not the dominant Hg methylators in this system. This work by MacMillan et al. highlights the emerging concern that in sensitive Arctic and Antarctic regions, a changing climate may lead to the release of stored legacy pollutants.

Fig. 3 Correlations between MeHg concentrations for surface waters sampled and (a) dissolved organic carbon (DOC), (b) total nitrogen (TN), (c) CO₂, (d) CH₄, (e) pH, and (f) SO₄²⁻. Circles represent the Bylot site and triangles represent Kuujjuarapik (excluding thaw pond bottom waters). Significant correlations were found for DOC, TN, CO₂ and CH₄. Reproduced with permission from G. A. MacMillan, C. Girard, J. Chételat, I. Laurion and M. Amyot, Environ. Sci. Technol., 2015, 49, 7743–7753. Copyright 2015 American Chemical Society.

Hg speciation and microbial productivity affect MeHg production

It is well established that net Hg methylation correlates with Hg speciation as well as factors that alter the anaerobic microbial community (Selin, Ann. Rev. Environ. Resour., 2009, 34, 43). Already in this Highlight, we have seen two in situ examples where alterations in the input of organic matter, Hg, or other mineral phases can have pronounced effects on net MeHg production. While these correlations are clear, the relative importance of microbial activity and Hg speciation is not well understood. In a recent publication, Kucharzyk et al. assess the relative importance of microbial productivity and Hg speciation by performing laboratory experiments with mixed sediment cultures (Kucharzyk et al., Environ. Sci.: Processes Impacts, 2015, 17, 1568). In their work, mixed cultures were first obtained by incubating sediment slurries taken from anoxic conditions under sulfate reducing conditions. The mixed cultures were then used in experiments with varying carbon substrate concentration and Hg speciation (dissolved Hg or nanoparticulate HgS). Microbial production and MeHg formation was then monitored in the cultures as they were incubated under sulfate reducing conditions. Results showed that the highest MeHg production was seen in the incubations with the highest added carbon content, regardless of the Hg speciation (Fig. 4). The presence of dissolved Hg, which is more bioavailable than HgS, led to enhanced production of MeHg in all cases. The differences observed in MeHg production with dissolved and nanoparticulate Hg incubations were less pronounced at lower carbon concentrations. To better quantify the action of sulfate reducing bacteria, sulfate consumption and the abundance of sulfate reductase genes were followed. These data showed a positive correlation between sulfate reduction and MeHg production in the presence of dissolved Hg, but were less clear for the HgS incubations. Overall, the work by Kucharzyk et al. show that Hg methylation is enhanced by more bioavailable Hg under favorable microbial growth conditions, but becomes limited by microbial activity, not bioavailability under growth substrate limited conditions. These results may aid future remediation efforts, showing that when possible it may be more beneficial to eliminate organic carbon inputs rather than attempting to alter the mineral phase of Hg in contaminated sites.

Fig. 4 MeHg production as a function of incubation time for cultures grown under varying carbon substrate concentrations for (A and B) site 1 and (C and D) site 2 when (A and C) dissolved Hg or (B and D) nanoparticulate HgS are added. Reproduced from Kucharzyk et al. with permission from The Royal Society of Chemistry.

Concluding remarks

The research highlighted in these recent articles adds to our understanding of which factors influence the cycling of Hg, and in return allows for the proper management of Hg emissions and successful remediation efforts. Bravo et al. demonstrated that the release of dissolved iron from a sewage treatment plant had the unintended consequence of increasing the local burden of MeHg. MacMillan et al. showed that the warming of arctic environments might lead to higher releases of MeHg due to enhanced activity of microbes in permafrost thaw ponds. Finally, Kucharzyk et al. provide evidence that Hg methylation by sulfate reducing bacteria is limited by Hg speciation under high microbial production conditions, but is less dependent on the form of Hg when microbial production is slow.

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