ABSTRACT
Mercury (Hg) is a global pollutant and potent neurotoxin that bioaccumulates in food webs as monomethylmercury (MeHg). The production of MeHg is driven by anaerobic and Hg redox cycling pathways such as Hg reduction, which control the availability of Hg to methylators. Anaerobes play an important role in Hg reduction in methylation hotspots, yet their contributions remain underappreciated due to how challenging these pathways are to study in the absence of dedicated genetic targets and low levels of Hg0 in anoxic environments. In this study we used Hg stable isotope fractionation to explore Hg reduction during anoxygenic photosynthesis and fermentation in the model anaerobe Heliobacterium modesticaldum Ice1. We show that cells preferentially reduce lighter Hg isotopes in both metabolisms leading to mass-dependent fractionation, but mass-independent fractionation commonly induced by UV-visible light is absent. Due to variability associated with replicated experiments, we could not discern whether dedicated physiological processes drive Hg reduction during photosynthesis and fermentation. However, we demonstrate that fractionation is affected by the interplay between pathways controlling Hg recruitment, accessibility, and availability alongside metabolic redox reactions. The combined contributions of these processes lead to isotopic enrichment during anoxygenic photosynthesis that is in between the values reported for anaerobic respiratory microbial Hg reduction and abiotic photoreduction. Isotope enrichment during fermentation is closer to what has been observed in aerobic bacteria that reduce Hg through dedicated detoxification pathways. Our work suggests that similar controls likely underpin diverse microbe-mediated Hg transformations that affect Hg’s fate in oxic and anoxic habitats.
IMPORTANCE Anaerobic and photosynthetic bacteria that reduce mercury affect mercury delivery to microbes in methylation sites that drive bioaccumulation in food webs. Anaerobic mercury reduction pathways remain underappreciated in the current view of the global mercury cycle because they are challenging to study, bearing no dedicated genetic targets to establish physiological mechanisms. In this study we used stable isotopes to characterize the physiological processes that control mercury reduction during photosynthesis and fermentation in the model anaerobe Heliobacterium modesticaldum Ice1. The sensitivity of isotope analyses highlighted the subtle contribution of mercury uptake towards the isotope signature associated with anaerobic mercury reduction. When considered alongside the isotope signatures associated with microbial pathways for which genetic determinants have been identified, our findings underscore the narrow range of isotope enrichment that is characteristic of microbial mercury transformations. This suggests that there exist common atomic-level controls for biological mercury transformations across a broad range of geochemical conditions.
Competing Interest Statement
The authors have declared no competing interest.
Footnotes
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We have edited our manuscript to state that we could not test whether common physiological mechanisms control Hg reduction during fermentation and anoxygenic photosynthesis. Given that this is the first report of an isotope enrichment signature for fermentative Hg reduction, we provide additional arguments in our manuscript as to why including these findings will advance the field of Hg biogeochemistry. We have provided additional details on the experimental setups employed to grow photosynthetic and fermentative cultures and how these conditions were designed to limit the contributions of abiotic processes to Hg isotope fractionation. We have also revised how we present the compilation of isotope enrichment signatures to facilitate visual interpretation (Figure 3). We have detailed all steps taken to compare isotope data in an effort to address this discrepancy within the field of isotope geochemistry (Table S5). We have separated our discussions surrounding physiological mechanisms affecting Hg isotope fractionation during photosynthesis and fermentation. We have also revised our conclusion to highlight the main findings from our experiments. We have moved figures to the end of the manuscript, remove captions for supporting figures, and revised the bibliography.