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

Abstract

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 or μmol L 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.

Algal Bloom Exacerbates Hydrogen Sulfide and Methylmercury Contamination in the Emblematic High-Altitude Lake Titicaca

“…Although MMHg is also low in concentration, a striking feature is a high percentage in MMHg which rises up to 20% while in non-contaminated surface waters around the globe it generally stands around 1-2%. As discussed in a previous publication [57], these high MMHg percentages can be explained by (i) high MMHg production in an environment favorable to methylating micro-organisms (e.g., sulfate-rich water and sediment, lower dissolved oxygen levels, neutral to alkaline water, shallow areas, et al) [92], (ii) stabilization and accumulation of MMHg in waters due to abundant (in)organic ligands [105], and (iii) low degradation of MMHg in organic-rich waters.…”

“…High sulfate levels in the systems that prompt SRB dominance under low oxygen conditions, as shown by the high H 2 S concentrations, may explain the observed increase of MMHg in the water [92]. SRB are the main Hg methylators at Titicaca Lake [105]. However, several studies have suggested that blooms may reduce MMHg concentrations in algae by a biomass growth dilution effect and have shown observationally [106] and experimental data [6,7,107] to support such a hypothesis.…”

“…So, our results support such recent modeling projections ( Figure 5A). It seems that under sulfate-rich conditions a bloom generates the ideal conditions for SRB, the principal Hg methylators [105], to thrive and generate not only high H 2 S concentrations but also higher MMHg concentrations. The effect of the bloom on the oxygen profile ( Figure 2) may have allowed SRB to move the periphyton and biofilms associated with sediments [105] to the water column.…”

“…It seems that under sulfate-rich conditions a bloom generates the ideal conditions for SRB, the principal Hg methylators [105], to thrive and generate not only high H 2 S concentrations but also higher MMHg concentrations. The effect of the bloom on the oxygen profile ( Figure 2) may have allowed SRB to move the periphyton and biofilms associated with sediments [105] to the water column. Also, abundant ligands present in these alkaline waters have likely favored the stabilization of MMHg in surface waters [57].…”

Long-Term Effects of Mercury on Biofilms Grown in Contaminated Microcosms: A Pilot Study

“…They are recognized to participate in the transformations of Hg in natural waters. Indeed, bioaccumulated IHg has been demonstrated to be reduced into its elemental Hg 0 form by biofilms [12] as well as methylated by inhabiting sulfate-reducing bacteria, iron-reducing bacteria, and methanogens whereas demethylation of MeHg has been also shown to occur [13][14][15].…”