Swift evolutionary response of microbes to a rise in anthropogenic mercury in the Northern Hemisphere

Anthropogenic mercury remobilization has considerably increased since the Industrial Revolution in the late 1700s. The Minamata Convention on Mercury is a United Nations treaty (2017) aiming at curbing mercury emissions. Unfortunately, evaluating the effectiveness of such a global treaty is hampered by our inability to determine the lag in aquatic ecosystem responses to a change in atmospheric mercury deposition. Whereas past metal concentrations are obtained from core samples, there are currently no means of tracking historical metal bioavailability or toxicity. Here, we recovered DNA from nine dated sediment cores collected in Canada and Finland, and reconstructed the past demographics of microbes carrying genes coding for the mercuric reductase (MerA)—an enzyme involved in Hg detoxification—using Bayesian relaxed molecular clocks. We found that the evolutionary dynamics of merA exhibited a dramatic increase in effective population size starting from 1783.8 ± 3.9 CE, which coincides with both the Industrial Revolution, and with independent measurements of atmospheric Hg concentrations. We show that even low levels of anthropogenic mercury affected the evolutionary trajectory of microbes in the Northern Hemisphere, and that microbial DNA encoding for detoxification determinants stored in environmental archives can be used to track historical pollutant toxicity.