Mechanisms Regulating Mercury Bioavailability for Methylating Microorganisms in the Aquatic Environment: A Critical Review Heileen Hsu-Kim,* Katarzyna H. Kucharzyk, Tong Zhang, and Marc A. Deshusses Department of Civil and Environmental Engineering, Duke University, 121 Hudson Hall, Box 90287, Durham, North Carolina 27708, United States ABSTRACT: Mercury is a potent neurotoxin for humans, partic- ularly if the metal is in the form of methylmercury. Mercury is widely distributed in aquatic ecosystems as a result of anthropogenic activities and natural earth processes. A first step toward bioaccumulation of methylmercury in aquatic food webs is the methylation of inorganic forms of the metal, a process that is primarily mediated by anaerobic bacteria. In this Review, we evaluate the current state of knowledge regarding the mechanisms regulating microbial mercury methylation, including the speciation of mercury in environments where methylation occurs and the processes that control mercury bioavailability to these organisms. Methylmercury production rates are generally related to the presence and productivity of methylating bacteria and also the uptake of inorganic mercury to these microorganisms. Our understanding of the mechanisms behind methylation is limited due to fundamental questions related to the geochemical forms of mercury that persist in anoxic settings, the mode of uptake by methylating bacteria, and the biochemical pathway by which these microorganisms produce and degrade methylmercury. In anoxic sediments and water, the geochemical forms of mercury (and subsequent bioavailability) are largely governed by reactions between Hg(II), inorganic sulfides, and natural organic matter. These interactions result in a mixture of dissolved, nanoparticulate, and larger crystalline particles that cannot be adequately represented by conventional chemical equilibrium models for Hg bioavailability. We discuss recent advances in nanogeochemistry and environmental microbiology that can provide new tools and unique perspectives to help us solve the question of how microorganisms methylate mercury. An understanding of the factors that cause the production and degradation of methylmercury in the environment is ultimately needed to inform policy makers and develop long-term strategies for controlling mercury contamination. 1. INTRODUCTION Mercury (Hg) is a global pollutant that is released from both natural and anthropogenic sources. 1 Molecules and materials containing this trace element can spread widely in the nature (even in remote areas) through a complex web of trans- formation and transport processes. In most environmental settings, mercury exists as the elemental form Hg 0 , inorganic divalent Hg(II), and organomercury compounds, such as monomethylmercury (MeHg). Each form of mercury can impart health hazards, depending on the dose and route of exposure. MeHg is the species of most concern for humans 2 because of the highly bioaccumulative nature of this organo- mercurial compound. 3 The neurotoxic effects of MeHg to humans, particularly during early stages of brain development, have been well-documented. 4,5 Moreover, exposure rates to vulnerable portions of the population (maternal age women and newborn children) can be considerable. In the U.S. for example, maternal exposure rates suggest that tens of thousands to hundreds of thousands of children are born each year with in utero MeHg exposures exceeding health guidelines. 5,6 Maternal consumption of fish is believed to be the major route of exposure for newborns. Because of the health risks, millions of river miles and lake acres in the U.S. have been placed under fish consumption advisories, 7 indicating the widespread prevalence and persistence of methylmercury contamination in the environment. The methylation of mercury in the aquatic environment is a critical step toward accumulation of this toxic metal in the aquatic food chain. MeHg is produced in the environment primarily by anaerobic bacteria that exist in most natural settings. MeHg levels in aquatic systems vary widely and do not necessarily correlate to the total amount of mercury in water or sediments. 8 Instead, mercury methylation rates generally depend on the productivity of the anaerobic microorganisms that can methylate mercury and the bioavailability of inorganic Hg(II) that can be taken up by these bacteria. 9-11 The processes that result in elevated methylmercury concentrations in the environment have received much attention in the last three decades, yet much is unknown concerning the forms of inorganic mercury that are available for methylation and the biochemical mechanisms by which Received: February 19, 2012 Revised: January 26, 2013 Accepted: February 5, 2013 Published: February 5, 2013 Critical Review pubs.acs.org/est © 2013 American Chemical Society 2441 dx.doi.org/10.1021/es304370g | Environ. Sci. Technol. 2013, 47, 2441-2456