In Situ Photochemical Transformation of Hg Species and Associated Isotopic Fractionation in the Water Column of High-Altitude Lakes from the Bolivian Altiplano.

Photochemical reactions are major pathways for the removal of Hg species from aquatic ecosystems, lowering the concentration of monomethylmercury (MMHg) and its bioaccumulation in foodwebs. Here, we investigated the rates and environmental drivers of MMHg photodegradation and inorganic Hg (IHg) photoreduction in waters of two high-altitude lakes from the Bolivian Altiplano representing meso- to eutrophic conditions. We incubated three contrasting waters in situ at two depths after adding Hg-enriched isotopic species to derive rate constants. We found that transformations mostly occurred in subsurface waters exposed to UV radiation and were mainly modulated by the dissolved organic matter (DOM) level. In parallel, we incubated the same waters after the addition of low concentrations of natural MMHg and followed the stable isotope composition of the remaining Hg species by compound-specific isotope analysis allowing the determination of enrichment factors and mass-independent fractionation (MIF) slopes (Δ199Hg/Δ201Hg) during in situ MMHg photodegradation in natural waters. We found that MIF enrichment factors potentially range from -11 to -19‰ and average -14.3 ± 0.6‰ (1 SE). The MIF slope diverged depending on the DOM level, ranging from 1.24 ± 0.03 to 1.34 ± 0.02 for the low and high DOM waters, respectively, and matched the MMHg MIF slope recorded in fish from the same lake. Our in situ results thus reveal (i) a relatively similar extent of Hg isotopic fractionation during MMHg photodegradation among contrasted natural waters and compared to previous laboratory experiments and (ii) that the MMHg MIF recorded in fish is characteristic for the MMHg bonding environment. They will enable a better assessment of the extent and conditions conducive to MMHg photodegradation in aquatic ecosystems.

Preferential Liver Accumulation of Mercury Explains Low Concentrations in Muscle of Caiman yacare (Alligatoridae) in Upper Amazon.

Caiman yacare is considered one of the top predators in the Amazon basin, and understanding pollutant distribution within its tissues may help its sustainable management. As a top predator, C. yacare should have the highest mercury concentrations, but has lower Hg concentrations than carnivorous fish (Rivera et al. 2016), which are part of their diet. We compared total Hg among liver, kidney, fat, and muscle of C. yacare, and whether trends in the distribution of Hg among tissues were like other crocodilians, aquatic birds, omnivorous, and carnivorous fish. Fat had the lowest concentrations (0.025 ± 0.03 mg kg-1) followed by muscle (0.15 ± 0.06 mg kg-1), kidney (0.57 ± 0.30 mg kg-1) and liver (1.81 ± 0.80 mg kg-1). Such preferential accumulation makes C. yacare meat a safer alternative for human consumption than carnivorous fish. The relation between Hg accumulation in liver and muscle is highest in crocodilians, which has evolutive and environmental implications.

High methylmercury uptake by green algae in Lake Titicaca: Potential implications for remediation.

Anthropogenic pressure in the high altitude lakes such as Titicaca and Uru (Bolivia) may favor the production of methylmercury (MeHg) known to accumulate in trophic chains. Periphyton associated with emerged aquatic plants (totoras) from the lake shores accumulates and demethylates MeHg providing a potential cost-effective water treatment technique. In this laboratory study, we measured the MeHg uptake kinetics of a consortium of green algae isolated from Lake Titicaca totora's periphyton. The most abundant algal consortium, composed of Oedogonium spp., Chlorella spp., Scenedesmus spp., was exposed to rising MeHg concentrations (from 5 to 200 ng·L-1) to assess their maximum potential capacity for MeHg accumulation. Various algal biomass concentrations were tested to choose the optimal one. Results provided a net MeHg uptake rate by this algal consortium of 2.38 amol ng-1·h-1·nM-1 (the total uptake was 2863 ng MeHg·g-1) for an initial concentration of 200 ng MeHg·L-1 with an algal biomass concentration of 0.02 g·L-1. This initial MeHg concentration is 1000 times higher than the one measured in the eutrophic Cohana Bay of Lake Titicaca, which shows the high accumulation potential of these green algae. Our data suggest that periphyton has a high potential for the treatment of Hg contaminated waters in constructing wetlands in the Andean Altiplano.

Extreme Arsenic Bioaccumulation Factor Variability in Lake Titicaca, Bolivia.

Latin America, like other areas in the world, is faced with the problem of high arsenic (As) background in surface and groundwater, with impacts on human health. We studied As biogeochemical cycling by periphyton in Lake Titicaca and the mine-impacted Lake Uru Uru. As concentration was measured in water, sediment, totora plants (Schoenoplectus californicus) and periphyton growing on stems, and As speciation was determined by X-ray absorption spectroscopy in bulk and EDTA-extracted periphyton. Dissolved arsenic was between 5.0 and 15 µg L-1 in Lake Titicaca and reached 78.5 µg L-1 in Lake Uru Uru. As accumulation in periphyton was highly variable. We report the highest As bioaccumulation factors ever measured (BAFsperiphyton up to 245,000) in one zone of Lake Titicaca, with As present as As(V) and monomethyl-As (MMA(V)). Non-accumulating periphyton found in the other sites presented BAFsperiphyton between 1281 and 11,962, with As present as As(III), As(V) and arsenosugars. DNA analysis evidenced several taxa possibly related to this phenomenon. Further screening of bacterial and algal isolates would be necessary to identify the organism(s) responsible for As hyperaccumulation. Impacts on the ecosystem and human health appear limited, but such organisms or consortia would be of great interest for the treatment of As contaminated water.

Linking Microbial Activities and Low-Molecular-Weight Thiols to Hg Methylation in Biofilms and Periphyton from High-Altitude Tropical Lakes in the Bolivian Altiplano.

The sources and factors controlling concentrations of monomethylmercury (MMHg) in aquatic ecosystems need to be better understood. Here, we investigated Hg transformations in sediments, periphyton associated with green algae's or aquatic plants, and benthic biofilms from the Lake Titicaca hydrosystem and compared them to the occurrence of active methylating microorganisms and extracellular Hg ligands. Intense Hg methylation was found in benthic biofilms and green algae's periphyton, while it remained low in sediments and aquatic plants' periphyton. Demethylation varied between compartments but remained overall in the same range. Hg methylation was mainly carried out by sulfate reducers, although methanogens also played a role. Its variability between compartments was first explained by the presence or absence of the hgcAB genes. Next, both benthic biofilm and green algae's periphyton exhibited a great diversity of extracellular low-molecular-weight (LMW) thiols (13 or 14 compounds) present at a range of a few nmol L-1 or µmol L-1 but clearly dominated by cysteine and 3-mercaptopropionic acid. Hg methylation was overall positively correlated to the total thiol concentrations, albeit to different extents according to the compartment and conditions. This work is the first examining the interplay between active methylating bacterial communities and extracellular ligands in heterotrophic biofilms and supports the involvement of LMW thiols in Hg methylation in real aquatic systems.

Challenges and opportunities for managing aquatic mercury pollution in altered landscapes.

The environmental cycling of mercury (Hg) can be affected by natural and anthropogenic perturbations. Of particular concern is how these disruptions increase mobilization of Hg from sites and alter the formation of monomethylmercury (MeHg), a bioaccumulative form of Hg for humans and wildlife. The scientific community has made significant advances in recent years in understanding the processes contributing to the risk of MeHg in the environment. The objective of this paper is to synthesize the scientific understanding of how Hg cycling in the aquatic environment is influenced by landscape perturbations at the local scale, perturbations that include watershed loadings, deforestation, reservoir and wetland creation, rice production, urbanization, mining and industrial point source pollution, and remediation. We focus on the major challenges associated with each type of alteration, as well as management opportunities that could lessen both MeHg levels in biota and exposure to humans. For example, our understanding of approximate response times to changes in Hg inputs from various sources or landscape alterations could lead to policies that prioritize the avoidance of certain activities in the most vulnerable systems and sequestration of Hg in deep soil and sediment pools. The remediation of Hg pollution from historical mining and other industries is shifting towards in situ technologies that could be less disruptive and less costly than conventional approaches. Contemporary artisanal gold mining has well-documented impacts with respect to Hg; however, significant social and political challenges remain in implementing effective policies to minimize Hg use. Much remains to be learned as we strive towards the meaningful application of our understanding for stakeholders, including communities living near Hg-polluted sites, environmental policy makers, and scientists and engineers tasked with developing watershed management solutions. Site-specific assessments of MeHg exposure risk will require new methods to predict the impacts of anthropogenic perturbations and an understanding of the complexity of Hg cycling at the local scale.

Association of a Specific Algal Group with Methylmercury Accumulation in Periphyton of a Tropical High-Altitude Andean Lake.

Periphyton relevance for methylmercury (MeHg) production and accumulation are now well known in aquatic ecosystems. Sulfate-reducing bacteria and other microbial groups were identified as the main MeHg producers, but the effect of periphyton algae on the accumulation and transfer of MeHg to the food web remains little studied. Here we investigated the role of specific groups of algae on MeHg accumulation in the periphyton of Schoenoplectus californicus ssp. (Totora) and Myriophyllum sp. in Uru Uru, a tropical high-altitude Bolivian lake with substantial fishing and mining activities accruing around it. MeHg concentrations were most strongly related to the cell abundance of the Chlorophyte genus Oedogonium (r 2 = 0.783, p = 0.0126) and to no other specific genus despite the presence of other 34 genera identified. MeHg was also related to total chlorophyll-a (total algae) (r 2 = 0.675, p = 0.0459), but relations were more significant with chlorophyte cell numbers, chlorophyll-b (chlorophytes), and chlorophyll-c (diatoms and dinoflagellates) (r 2 = 0.72, p = 0.028, r 2 = 0.744, p = 0.0214, and r 2 = 0.766, p = 0.0161 respectively). However, Oedogonium explains most variability of chlorophytes and chlorophyll-c (r 2 = 0.856, p = < 0.001 and r 2 = 0.619, p = 0.002, respectively), suggesting it is the most influential group for MeHg accumulation and periphyton algae composition at this particular location and given time.

Mercury methylation and hydrogen sulfide production among unexpected strains isolated from periphyton of two macrophytes of the Amazon.

The periphyton of macrophytes had previously been identified as important spots for mercury methylation in the Amazon basin, but the microorganisms that facilitate methylation in such compartment are still to be identified. Here, bacteria were isolated from periphyton associated with Eichhornia crassipes and Polygonum densiflorum in Widdel and Pfennig medium and tested for mercury methylation with a stable isotope tracer technique using (198)HgCl, hydrogen sulfide production and molybdate inhibition. Three Pleomorphomona spp., one unidentified Deltaproteobacteria, two Klebsiella spp., and one Tolumonas sp. were isolated. All except Tolumonas sp. were able to methylate mercury (up to 5% of the (198)HgCl added) and produce up to 4 mM of H(2)S, while the Deltaproteobacteria was also able to demethylate methylmercury. Although these bacteria may not be as strong mercury methylators as sulfate-reducing bacteria, they have the potential to contribute to methylmercury accumulation in the system.

Importance of sulfate reducing bacteria in mercury methylation and demethylation in periphyton from Bolivian Amazon region.

Sulfate reducing bacteria (SRB) are important mercury methylators in sediments, but information on mercury methylators in other compartments is ambiguous. To investigate SRB involvement in methylation in Amazonian periphyton, the relationship between Hg methylation potential and SRB (Desulfobacteraceae, Desulfobulbaceae and Desulfovibrionaceae) abundance in Eichhornia crassipes and Polygonum densiflorum root associated periphyton was examined. Periphyton subsamples of each macrophyte were amended with electron donors (lactate, acetate and propionate) or inhibitors (molybdate) of sulfate reduction to create differences in SRB subgroup abundance, which was measured by quantitative real-time PCR with primers specific for the 16S rRNA gene. Mercury methylation and demethylation potentials were determined by a stable isotope tracer technique using 200HgCl and CH3(202)HgCl, respectively. Relative abundance of Desulfobacteraceae (<0.01-12.5%) and Desulfovibrionaceae (0.01-6.8%) were both highly variable among samples and subsamples, but a significant linear relationship (p<0.05) was found between Desulfobacteraceae abundance and net methylmercury formation among treatments of the same macrophyte periphyton and among all P. densiflorum samples, suggesting that Desulfobacteraceae bacteria are the most important mercury methylators among SRB families. Yet, molybdate only partially inhibited mercury methylation potentials, suggesting the involvement of other microorganisms as well. The response of net methylmercury production to the different electron donors and molybdate was highly variable (3-1104 pg g(-1) in 12 h) among samples, as was the net formation in control samples (17-164 pg g(-1) in 12 h). This demonstrates the importance of community variability and complexity of microbial interactions for the overall methylmercury production in periphyton and their response to external stimulus.

Sulfate-reducing bacteria in floating macrophyte rhizospheres from an Amazonian floodplain lake in Bolivia and their association with Hg methylation.

Five subgroups of sulfate-reducing bacteria (SRB) were detected by PCR in three macrophyte rhizospheres (Polygonum densiflorum, Hymenachne donacifolia, and Ludwigia helminthorriza) and three subgroups in Eichhornia crassipes from La Granja, a floodplain lake from the upper Madeira basin. The SRB community varied according to the macrophyte species but with different degrees of association with their roots. The rhizosphere of the C4 plant Polygonum densiflorum had higher frequencies of SRB subgroups as well as higher mercury methylation potentials (27.5 to 36.1%) and carbon (16.06 +/- 5.40%), nitrogen (2.03 +/- 0.64%), Hg (94.50 +/- 6.86 ng Hg g(-1)), and methylmercury (8.25 +/- 1.45 ng Hg g(-1)) contents than the rhizosphere of the C3 plant Eichhornia crassipes. Mercury methylation in Polygonum densiflorum and Eichhornia crassipes was reduced when SRB metabolism was inhibited by sodium molybdate.