Simultaneous Reduction\nand Methylation of Nanoparticulate\nMercury: The Critical Role of Extracellular Electron Transfer

Mercury nanoparticles are abundant in natural environments.\nYet,\nunderstanding their contribution to global biogeochemical cycling\nof mercury remains elusive. Here, we show that microbial transformation\nof nanoparticulate divalent mercury can be an important source of\nelemental and methylmercury.Geobacter sulfurreducensPCA, a model bacterium predominant in anoxic environments (e.g.,\npaddy soils), simultaneously reduces and methylates nanoparticulate\nHg(II). Moreover, the relative prevalence of these two competing processes\nand the dominant transformation pathways differ markedly between nanoparticulate\nHg(II) and its dissolved and bulk-sized counterparts. Notably, even\nwhen intracellular reduction of Hg(II) nanoparticles is constrained\nby cross-membrane transport (a rate-limiting step that also regulates\nmethylation), the overall Hg(0) formation remains substantial due\nto extracellular electron transfer. With multiple lines of evidence\nbased on microscopic and electrochemical analyses, gene knockout experiments,\nand theoretical calculations, we show that nanoparticulate Hg(II)\nis preferentially associated with <i>c</i>-type cytochromes\non cell membranes and has a higher propensity for accepting electrons\nfrom the heme groups than adsorbed ionic Hg(II), which explains the\nsurprisingly larger extent of reduction of nanoparticles than dissolved\nHg(II) at relatively high mercury loadings. These findings have important\nimplications for the assessment of global mercury budgets as well\nas the bioavailability of nanominerals and mineral nanoparticles.