MICROBIAL TIME MACHINES: TOOLS TO INVESTIGATE THE PAST AND PRESENT OF MERCURY BIOGEOCHEMISTRY

Because of the complexity of its biogeochemical cycle, time lags in the response of many freshwater ecosystems to changes in atmospheric Hg levels can be expected, hampering our ability to manage Hg contamination. This inability to properly describe ecological linkages between historical changes in Hg deposition and ecosystem response has been identified as a major research gap in the latest United Nation Environment Program Global Mercury Assessment. We show that DNA extracted from sedimentary archives can inform on the response of microbes to historical Hg delivery. We observe a significant association between the mercuric reductase gene (merA) phylogeny and the timing of Hg deposition. Using relaxed molecular clock models, we show a significant increase in the population of detoxifying prokaryotes beginning ~200 years ago, coinciding with the Industrial Revolution and a coincident strong signal for positive selection acting on residues in the terminal region of the mercuric reductase. This rapid evolutionary response of microbes to changes in the delivery of anthropogenic Hg indicates that microbial genomes record ecosystem response to pollutant deposition in remote regions. While Hg methylation is often cited as one of the most important reactions occurring in anoxia, one outstanding question in Hg biogeochemistry pertains to the nature of Hg species available to methylating microbes. More importantly, we know very little about ecosystem pathways contributing to transform Hg into its bioavailable forms. While DNA extracted from sedimentary archives offers a window into Hg’s past, genetically modified biosensors offer contemporary insights into how Hg interacts with microbial cells. We show that such tools are now available to investigate Hg cycling in both aerobic and anaerobic conditions and discuss the role of dissolved organic matter as a key ligand affecting Hg’s fate in the environment.