Gregoire, D. S. | Search bioRxiv

bioRxiv2023

Microbial methane cycling in a landfill on a decadal time scale

Landfills generate outsized environmental footprints due to microbial degradation of organic matter in municipal solid waste, which produces the potent greenhouse gas methane. With global solid waste production predicted to increase 69% by the year 2050, there is a pressing need to better understand the biogeochemical processes that control microbial methane cycling in landfills. In this study, we had the rare opportunity to characterize the microbial community responsible for methane cycling in landfill waste covering a 39-year timeframe. We coupled long term geochemical analyses to whole-community DNA (i.e., metagenomic) sequencing and identified key features that shape methane cycling communities over the course of a landfills lifecycle. Anaerobic methanogenic microbes are more abundant, diverse, and metabolically versatile in newer waste, fueling rapid methane production early in a landfills lifecycle. Aerobic methanotrophs were repeatedly found in leachate where low levels of oxygen were present and exhibited adaptations that aid survival under steep redox gradients in landfills. The potential for anaerobic methane oxidation, which has historically been overlooked despite anoxic habitats dominating landfills, was prevalent in a 26-year-old landfill cell which was in a state of slow methanogenesis. Finally, we identified the metabolic potential for methane oxidation in lineages that are widespread in aquatic and terrestrial habitats, whose capacity to metabolize methane remains poorly characterized. Ultimately, this work expands the diversity of methane cycling guilds in landfills and outlines how these communities can curb methane emissions from municipal solid waste. SignificanceMicrobes are major contributors to methane emissions from solid waste however the temporal dynamics of methane cycling communities in landfills remain poorly understood. We addressed this gap by using whole-community DNA (i.e., metagenomic) approaches to characterize microbial methane cycling in waste covering a 39-year timeframe. We show that methane-producing microbes are more abundant, diverse, and metabolically versatile in new waste compared to old waste. We highlight that methane oxidation in the absence of oxygen is overlooked in landfill biogeochemical models and that novel lineages can potentially contribute to methane sinks across a broad range of habitats. These findings can strengthen predictive models for methane cycling in landfills and inform sustainable waste management strategies to curb methane emissions from solid waste.

microbiology↗

bioRxiv2020

Common physiological processes control mercury reduction during photosynthesis and fermentation

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. We show that isotope 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. These results demonstrate that common controls exist at the atomic level for Hg reduction during photosynthesis and fermentation in H. modesticaldum. Our work suggests that similar controls likely underpin diverse microbe-mediated Hg transformations that affect Hgs fate in oxic and anoxic habitats. IMPORTANCEAnaerobic 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 show that common physiological processes 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.

microbiology↗