Amina T. Schartup

Methylmercury Production in Estuarine Sediments: Role of Organic Matter

Methylmercury (MeHg) affects wildlife and human health mainly through marine fish consumption. In marine systems, MeHg is formed from inorganic mercury (Hg(II)) species primarily in sediments, then accumulates and biomagnifies in the food web. Most of the fish consumed in the United States are from estuarine and marine systems, highlighting the importance of understanding MeHg formation in these productive regions. Sediment organic matter has been shown to limit mercury methylation in estuarine ecosystems, as a result it is often described as the primary control over MeHg production. In this paper, we explore the role of organic matter by looking at the effects of its changing sediment concentrations on the methylation rates across multiple estuaries. We measured sedimentary MeHg production at eleven estuarine sites that were selected for their contrasting biogeochemical characteristics, mercury (Hg) content, and location in the Northeastern U.S. (ME, NH, CT, NY, and NJ). Sedimentary total Hg concentrations ranged across 5 orders of magnitude, increasing in concentration from the pristine, sandy sediments of Wells (ME), to industrially contaminated areas such as Portsmouth (NH) and Hackensack (NJ). We find that methylation rates are the highest at locations with high Hg content (relative to carbon), and that organic matter does not hinder mercury methylation in estuaries.

Contrasting Effects of Marine and Terrestrially Derived Dissolved Organic Matter on Mercury Speciation and Bioavailability in Seawater

Methylmercury (MeHg) is the only species of mercury (Hg) to biomagnify in aquatic food-webs to levels that are a widespread concern for human and ecological health. Here we investigate the association between dissolved organic matter (DOM) in seawater and Hg speciation and uptake using experimental data and field measurements from Long Island Sound (LIS) and the Northwestern Atlantic continental margin. We measured differences in DOM composition across sampling stations using excitation emission matrix fluorescence spectroscopy and further separated DOM into terrestrial and marine components using Parallel Factor Analysis (PARAFAC). Highest MeHg concentrations were found in the estuarine stations (LIS) with highest DOM concentrations due to enhanced external inputs from the watershed and rivers. For stations on the shelf and slope, MeHg in plankton increased linearly with a decreasing fraction of fluorescence attributable to DOM components with a terrestrial rather than marine origin. These results are corroborated by experimental data showing higher MeHg uptake by cells in the presence of predominantly marine DOM compared to terrestrial DOM. Highest fractions of dissolved gaseous mercury were also found at stations with the highest marine DOM content, suggesting a greater reducible fraction of divalent inorganic Hg. These data suggest DOM composition is a critical driver of Hg reactivity and bioavailability in offshore marine waters.

Freshwater discharges drive high levels of methylmercury in Arctic marine biota

Significance Estuaries are the predominant hunting and fishing territory for northern indigenous populations whose way of life is threatened by both climate change and industrial development. Direct measurements and modeling conducted as part of this study show enhanced production of methylmercury, a potent neurotoxin, and uptake by plankton in stratified oxic seawater. Enhanced climate-driven stratification of ocean margin areas with sea-ice melt will likely elevate biological methylmercury concentrations in the Arctic. Elevated biological methylmercury levels will be exacerbated by hydroelectric development planned throughout many northern regions. Our experimental measurements indicate that, over the next decade, regional increases in methylmercury concentrations resulting from flooding associated with hydroelectric development will be greater than those expected from climate change. Elevated levels of neurotoxic methylmercury in Arctic food-webs pose health risks for indigenous populations that consume large quantities of marine mammals and fish. Estuaries provide critical hunting and fishing territory for these populations, and, until recently, benthic sediment was thought to be the main methylmercury source for coastal fish. New hydroelectric developments are being proposed in many northern ecosystems, and the ecological impacts of this industry relative to accelerating climate changes are poorly characterized. Here we evaluate the competing impacts of climate-driven changes in northern ecosystems and reservoir flooding on methylmercury production and bioaccumulation through a case study of a stratified sub-Arctic estuarine fjord in Labrador, Canada. Methylmercury bioaccumulation in zooplankton is higher than in midlatitude ecosystems. Direct measurements and modeling show that currently the largest methylmercury source is production in oxic surface seawater. Water-column methylation is highest in stratified surface waters near the river mouth because of the stimulating effects of terrestrial organic matter on methylating microbes. We attribute enhanced biomagnification in plankton to a thin layer of marine snow widely observed in stratified systems that concentrates microbial methylation and multiple trophic levels of zooplankton in a vertically restricted zone. Large freshwater inputs and the extensive Arctic Ocean continental shelf mean these processes are likely widespread and will be enhanced by future increases in water-column stratification, exacerbating high biological methylmercury concentrations. Soil flooding experiments indicate that near-term changes expected from reservoir creation will increase methylmercury inputs to the estuary by 25–200%, overwhelming climate-driven changes over the next decade.

A mass budget for mercury and methylmercury in the Arctic Ocean

Elevated biological concentrations of methylmercury (MeHg), a bioaccumulative neurotoxin, are observed throughout the Arctic Ocean, but major sources and degradation pathways in seawater are not well understood. We develop a mass budget for mercury species in the Arctic Ocean based on available data since 2004 and discuss implications and uncertainties. Our calculations show that high total mercury (Hg) in Arctic seawater relative to other basins reflect large freshwater inputs and sea ice cover that inhibits losses through evasion. We find that most net MeHg production (20 Mg a−1) occurs in the subsurface ocean (20–200 m). There it is converted to dimethylmercury (Me2Hg: 17 Mg a−1), which diffuses to the polar mixed layer and evades to the atmosphere (14 Mg a−1). Me2Hg has a short atmospheric lifetime and rapidly degrades back to MeHg. We postulate that most evaded Me2Hg is redeposited as MeHg and that atmospheric deposition is the largest net MeHg source (8 Mg a−1) to the biologically productive surface ocean. MeHg concentrations in Arctic Ocean seawater are elevated compared to lower latitudes. Riverine MeHg inputs account for approximately 15% of inputs to the surface ocean (2.5 Mg a−1) but greater importance in the future is likely given increasing freshwater discharges and permafrost melt. This may offset potential declines driven by increasing evasion from ice-free surface waters. Geochemical model simulations illustrate that for the most biologically relevant regions of the ocean, regulatory actions that decrease Hg inputs have the capacity to rapidly affect aquatic Hg concentrations.

Sediment-porewater partitioning, total sulfur, and methylmercury production in estuaries.

Mercury (Hg) speciation and the activity of Hg(II)-methylating bacteria are responsible for the rate of methylmercury production and thus bioaccumulation in marine foodwebs. Factors affecting porewater partitioning (Kd) and methylation of Hg(II) were examined at 11 sites in sediment of 4 biogeochemically diverse estuaries in the Northeast U.S. In Long Island Sound, 88% of total mercury (HgT) log Kd variability was described by porewater dissolved organic carbon concentration and sediment total sulfur (S) content. Whereas across all estuaries, regression analyses showed that S alone drives about 70% of Kd variability and 50% of changes in methylation rates; and the inclusion of DOC and sulfides did not improve the prediction. Thus, we demonstrated that S is a better predictor of HgT log Kd than the sediment organic matter across multiple estuaries, and while organic matter and S are interchangeable in small-scale studies, on a larger scale, sediment S content is the simplest and most effective variable to measure.

Seasonal Cycling and Transport of Mercury and Methylmercury in the Turbidity Maximum of the Delaware Estuary

The Delaware River Estuary (DRE) is a cornerstone of industrialization, shipping, and urban usage, and has a long history of human impact on pollution and recovery. Mercury (Hg) is a contaminant of concern in the DRE based upon concentrations in some fish samples that were found to exceed State and Federal fish tissue criteria. Methylation of Hg often follows a seasonal pattern as its production is biologically mediated. Surveys were conducted in November 2011, April 2012, and July 2012 to assess this effect. We sampled surface and bottom water at six sites spanning the estuarine turbidity maximum (ETM) in the main channel of the river, plus three sediment sites at shallow, subtidal locations. Our results indicate there is a clear seasonal increase in both water column and sediment methylmercury (MeHg) and %MeHg concentrations in the ETM during July. Water-column-filtered total mercury (HgT), suspended particle HgT, and MeHg concentrations were found to fluctuate little with location or season in the ETM. In contrast, sediment MeHg, water-column-filtered MeHg, and pore water HgT varied seasonally. Furthermore, pore water MeHg levels were elevated in concert with increased kmeth rates in July. Estimated river input and sediment and atmospheric depositional MeHg flux were compared seasonally. River flux was more than an order of magnitude higher than sediment flux in April, coinciding with higher fluvial transport. However, during July, river flux decreases and sediment flux becomes a larger relative source. This trend has potential implications for fish and other biota residing in the DRE during summer.

The use of a mercury biosensor to evaluate the bioavailability of mercury-thiol complexes and mechanisms of mercury uptake in bacteria

As mercury (Hg) biosensors are sensitive to only intracellular Hg, they are useful in the investigation of Hg uptake mechanisms and the effects of speciation on Hg bioavailability to microbes. In this study, bacterial biosensors were used to evaluate the roles that several transporters such as the glutathione, cystine/cysteine, and Mer transporters play in the uptake of Hg from Hg-thiol complexes by comparing uptake rates in strains with functioning transport systems to strains where these transporters had been knocked out by deletion of key genes. The Hg uptake into the biosensors was quantified based on the intracellular conversion of inorganic mercury (Hg(II)) to elemental mercury (Hg(0)) by the enzyme MerA. It was found that uptake of Hg from Hg-cysteine (Hg(CYS)2) and Hg-glutathione (Hg(GSH)2) complexes occurred at the same rate as that of inorganic complexes of Hg(II) into Escherichia coli strains with and without intact Mer transport systems. However, higher rates of Hg uptake were observed in the strain with a functioning Mer transport system. These results demonstrate that thiol-bound Hg is bioavailable to E. coli and that this bioavailability is higher in Hg-resistant bacteria with a complete Mer system than in non-resistant strains. No difference in the uptake rate of Hg from Hg(GSH)2 was observed in E. coli strains with or without functioning glutathione transport systems. There was also no difference in uptake rates between a wildtype Bacillus subtilis strain with a functioning cystine/cysteine transport system, and a mutant strain where this transport system had been knocked out. These results cast doubt on the viability of the hypothesis that the entire Hg-thiol complex is taken up into the cell by a thiol transporter. It is more likely that the Hg in the Hg-thiol complex is transferred to a transport protein on the cell membrane and is subsequently internalized.

A Model for Methylmercury Uptake and Trophic Transfer by Marine Plankton

Methylmercury (MeHg) concentrations can increase by 100 000 times between seawater and marine phytoplankton, but levels vary across sites. To better understand how ecosystem properties affect variability in planktonic MeHg concentrations, we develop a model for MeHg uptake and trophic transfer at the base of marine food webs. The model successfully reproduces measured concentrations in phytoplankton and zooplankton across diverse sites from the Northwest Atlantic Ocean. Highest MeHg concentrations in phytoplankton are simulated under low dissolved organic carbon (DOC) concentrations and ultraoligotrophic conditions typical of open ocean regions. This occurs because large organic complexes bound to MeHg inhibit cellular uptake and cell surface area to volume ratios are greatest under low productivity conditions. Modeled bioaccumulation factors for phytoplankton (102.4-105.9) are more variable than those for zooplankton (104.6-106.2) across ranges in DOC (40-500 μM) and productivities (ultraoligotrophic to hypereutrophic) typically found in marine ecosystems. Zooplankton growth dilutes their MeHg body burden, but they also consume greater quantities of MeHg enriched prey at larger sizes. These competing processes lead to lower variability in MeHg concentrations in zooplankton compared to phytoplankton. Even under hypereutrophic conditions, modeled growth dilution in marine zooplankton is insufficient to lower their MeHg concentrations, contrasting findings from freshwater ecosystems.

Biogeochemistry: Mercury methylation on ice

Metagenomic analysis of Antarctic sea-ice and brine reveals the presence of hgcAB-like genes in the microaerophilic marine bacterium Nitrospina. These are similar to ones responsible for mercury methylation in anaerobic microorganisms and provide a plausible mechanism for mercury methylation in oxic marine environments.