Mercury Methylation and Detoxification by Novel Microorganisms in Mercury Enriched Mesothermal Springs

Abstract:

Hot springs and fumaroles release significant quantities of aqueous and gaseous mercury into the environment. Yet few studies have looked at the microbial underpinnings of mercury transformations in geothermal settings. Recent advancements in culture-independent molecular techniques, such as ultra-high-throughput sequencing, allow us to delve deeply into the functional and phylogenetic make-up of these extreme environments. Here we present results from deep metagenomic sequencing of geothermal microbial communities cycling mercury, focussing on the connections between putative metabolisms and mercury methylation, and the evolution of the mer-operon. Presented are data from two adjacent, acidic (pH<3), mesothermal (33-68 °C) hot springs of the Ngawha geothermal field (New Zealand), extremely enriched in total mercury (>1000 ng L^-1), and varying methylmercury concentrations (1-10 ng L^-1). Microbial communities of both springs are dominated by mercury resistant acidophilic, sulfur- and iron-cycling microbes: Acidithiobacillus, Thiomonas, and Thermoplasma. Mercury methylation genes (hgcAB) were only detected in the cooler spring (∆T~10 °C), with an order of magnitude greater methylmercury (10 ng L^-1). The hgcAB genes have no known closest relatives (<90%), but lowest common ancestor analysis matched members of the Firmicutes and Deltaproteobacteria as well as uncultured environmental bacteria. Our findings show that geothermal microbial communities are capable of a net production of methylmercury, alongside active demethylation-reduction by mer-capable microbes, despite selective pressures from low pH and high mercury levels. However, temperature may be the major limiting factor on mercury biomethylation in geothermal settings, as no hgcAB genes were detected in the spring that was nearly identical in all physio-chemical parameters to its neighbour except for temperature (T >40°C), and methylmercury concentration. We conclude that the relative amount of mercury methylation in each hot spring is controlled by the presence of methylating bacteria and archaea, the release of bioavailable mercury species from sulfide minerals, counterbalanced by microbial mercury demethylation and reduction and mercury sulfide mineralization.