Microbial methylation and demethylation are two competing processes controlling the net production and bioaccumulation of neurotoxic methylmercury (MeHg) in natural ecosystems. Although mercury (Hg) methylation by anaerobic microorganisms and demethylation by aerobic Hg-resistant bacteria have both been extensively studied, little attention has been given to MeHg degradation by anaerobic bacteria, particularly the iron-reducing bacterium Geobacter bemidjiensis Bem. Here we report, for the first time, that the strain G. bemidjiensis Bem can mediate a suite of Hg transformations, including Hg(II) reduction, Hg(0) oxidation, MeHg production and degradation under anoxic conditions. Results suggest that G. bemidjiensis utilizes a reductive demethylation pathway to degrade MeHg, with elemental Hg(0) as the major reaction product, possibly due to the presence of genes encoding homologues of an organomercurial lyase (MerB) and a mercuric reductase (MerA). In addition, the cells can strongly sorb Hg(II) and MeHg, reduce or oxidize Hg, resulting in both time and concentration-dependent Hg species transformations. Moderate concentrations (10-500 μM) of Hg-binding ligands such as cysteine enhance Hg(II) methylation but inhibit MeHg degradation. These findings indicate a cycle of Hg methylation and demethylation among anaerobic bacteria, thereby influencing net MeHg production in anoxic water and sediments.

The fate of soil organic carbon (SOC) stored in the Arctic permafrost is a key concern as temperatures continue to rise in the northern hemisphere. Studies and conceptual models suggest that degradation of SOC is affected by its composition, but it is unclear exactly which SOC fractions are vulnerable to rapid breakdown and what mechanisms may be controlling SOC degradation upon permafrost thaw. Here, we examine the dynamic consumption and production of labile SOC in an anoxic incubation experiment using soil samples from the active layer at the Barrow Environmental Observatory, Barrow, Alaska, USA. Free-reducing sugars, alcohols, and low-molecular-weight (LMW) organic acids were analyzed during incubation at either-2 or 8 °C for up to 240 days. Results show that degradation of simple sugar and alcohol in SOC largely accounts for the initial rapid release of CO 2 and CH 4 through anaerobic fermentation, whereas the fermentation products, acetate and formate, are subsequently utilized as primary substrates for methanogenesis. Iron(III) reduction is correlated with acetate production and methanogenesis, suggesting its important role as an electron acceptor in SOC respiration in tundra environment. These observations are further supported in a glucose addition experiment, in which rapid CO 2 and CH 4 production occurred concurrently with rapid production and consumption of labile organics such as acetate. However, addition of tannic acid, as a more complex organic substrate, showed little influence on the overall production of CO 2 and CH 4 and organic acids. Together our study shows that LMW labile SOC controls the initial rapid release of greenhouse gases upon warming of permafrost soils. We present a conceptual framework for the labile SOC transformations and their relations to fermentation, iron reduction and methanogenesis, thereby providing the basis for improved model prediction of climate feedbacks in the Arctic.

Climate change is warming tundra ecosystems in the Arctic, resulting in the decomposition of previously-frozen soil organic matter (SOM) and release of carbon (C) to the atmosphere; however, the processes that control SOM decomposition and C emissions remain highly uncertain. In this study, we evaluate geochemical factors that influence microbial production of carbon dioxide (CO 2 ) and methane (CH 4 ) in the seasonally-thawed active layer of interstitial polygonal tundra near Barrow, Alaska. We report spatial and seasonal patterns of dissolved gases in relation to the geochemical properties of Fe and organic C in soil and soil solution, as determined using spectroscopic and chromatographic techniques. The chemical composition of soil water collected during the annual thaw season varied significantly with depth. Soil water in the middle of the active layer contained abundant Fe(III), and aromatic-C and low-molecularweight organic acids derived from SOM decomposition. At these depths, CH 4 was positively correlated with the ratio of Fe(III) to total Fe in waterlogged transitional and low-centered polygons but negatively correlated in the drier flat-and high-centered polygons. These observations contradict the expectation Responsible Editor: Stephen Porder.Electronic supplementary material The online version of this article (

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Arctic tundra soils store a large quantity of organic carbon that is susceptible to decomposition and release to the atmosphere as methane (CH 4 ) and carbon dioxide (CO 2 ) under a warming climate. Anaerobic processes that generate CH 4 and CO 2 remain unclear because previous studies have focused on aerobic decomposition pathways. To predict releases of CO 2 and CH 4 from tundra soils, it is necessary to identify pathways of soil organic matter decomposition under the anoxic conditions that are prevalent in Arctic ecosystems. Here molecular and spectroscopic techniques were used to monitor biological degradation of water-extractable organic carbon (WEOC) during anoxic incubation of tundra soils from a region of continuous permafrost in northern Alaska. Organic and mineral soils from the tundra active layer were incubated at À2, +4, or +8°C for up to 60 days to mimic the short-term thaw season. Results suggest that, under anoxic conditions, fermentation converted complex organic molecules into simple organic acids that were used in concomitant Fe-reduction and acetoclastic methanogenesis reactions. Nonaromatic compounds increased over time as WEOC increased. Organic acid metabolites initially accumulated in soils but were mostly depleted by day 60 because organic acids were consumed to produce Fe(II), CO 2 , and CH 4 . We conclude that fermentation of nonprotected organic matter facilitates methanogenesis and Fe reduction reactions, and that the proportion of organic acids consumed by methanogenesis increases relative to Fe reduction with increasing temperature. The decomposition pathways observed in this study are important to consider in numerical modeling of greenhouse gas production in the Arctic. HERNDON ET AL.BIOGEOCHEMISTRY OF ANOXIC ARCTIC TUNDRA 2345 PUBLICATIONS

Rapid temperature rise in Arctic permafrost impacts not only the degradation of stored soil organic carbon (SOC) and climate feedback, but also the production and bioaccumulation of methylmercury (MeHg) toxin that can endanger humans, as well as wildlife in terrestrial and aquatic ecosystems. Currently little is known concerning the effects of rapid permafrost thaw on microbial methylation and how SOC degradation is coupled to MeHg biosynthesis. Here we describe the effects of warming on MeHg production in an Arctic soil during an 8-month anoxic incubation experiment. Net MeHg production increased >10 fold in both organic- and mineral-rich soil layers at warmer (8 °C) than colder (-2 °C) temperatures. The type and availability of labile SOC, such as reducing sugars and ethanol, were particularly important in fueling the rapid initial biosynthesis of MeHg. Freshly amended mercury was more readily methylated than preexisting mercury in the soil. Additionally, positive correlations between mercury methylation and methane and ferrous ion production indicate linkages between SOC degradation and MeHg production. These results show that climate warming and permafrost thaw could potentially enhance MeHg production by an order of magnitude, impacting Arctic terrestrial and aquatic ecosystems by increased exposure to mercury through bioaccumulation and biomagnification in the food web.

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