Abstract
Humic substances are redox-active organic molecules, which play pivotal roles in several biogeochemical cycles due to their electron-transferring capacity involving multiple abiotic and microbial transformations. Based on the redox properties of humic substances, and the metabolic capabilities of microorganisms to reduce and oxidize them, we hypothesized that they could mediate the anaerobic oxidation of methane (AOM) coupled to the reduction of nitrous oxide (N2O) in wetland sediments. This study provides several lines of evidence indicating the coupling between AOM and the reduction of N2O through an extracellular electron transfer mechanism mediated by the redox active functional groups in humic substances (e.g., quinones). We found that the microbiota of a sediment collected from the Sisal wetland (Yucatán Peninsula, southeastern Mexico) was able to reduce N2O (4.6 ± 0.5 μmol N2O g sed.–1 day–1) when reduced humic substances were provided as electron donor in a close stoichiometric relationship. Furthermore, a microbial enrichment derived from the wetland sediment achieved simultaneous 13CH4 oxidation (1.3 ± 0.1 μmol 13CO2 g sed.–1 day–1) and N2O reduction (25.2 ± 0.5 μmol N2O g sed.–1 day–1), which was significantly dependent on the presence of humic substances as an extracellular electron shuttle. Taxonomic characterization based on 16S rRNA gene sequencing revealed Acinetobacter (a ɣ-proteobacterium), the Rice Cluster I from the Methanocellaceae and an uncultured archaeon from the Methanomicrobiaceae family as the microbes potentially involved in AOM linked to N2O reduction mediated by humic substances. The findings reported here suggest that humic substances might play an important role to prevent the emission of greenhouse gases (CH4 and N2O) from wetland sediments. Further efforts to evaluate the feasibility of this novel mechanism under the natural conditions prevailing in ecosystems must be considered in future studies.
Highlights
Continuous emissions of greenhouse gases (GHG), such as carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O) have been associated to several environmental problems that include global warming (GW), alterations of precipitation patterns, changes in groundwater levels and soil conditions, as well as extreme weather events (Kumar et al, 2020)
Taking into account the previous evidence showing that reduced humic substances could serve as electron donor for denitrification (Aranda-Tamaura et al, 2007; van Trump et al, 2011), and that oxidized humic substances could support anaerobic oxidation of methane (AOM) by serving as terminal electron acceptors (TEAs) (Valenzuela et al, 2017), we aimed to decipher if they could mediate AOM linked to N2O reduction via an inter-species electron transfer (IET) process
Bottles were vigorously shaken and 500 μL of slurry were taken with sterile disposable syringes to extract DNA using the PowerSoil DNA extraction kit (Mo Bio Laboratories, Carlsbad, CA, United States) according to the protocol described by the manufacturer
Summary
Continuous emissions of greenhouse gases (GHG), such as carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O) have been associated to several environmental problems that include global warming (GW), alterations of precipitation patterns, changes in groundwater levels and soil conditions, as well as extreme weather events (Kumar et al, 2020). Intensive research is currently underway to elucidate the microbial and abiotic processes driving these GHG emissions from natural environments. Wetlands are highly dynamic ecosystems that, collectively, constitute the largest biogenic source of GHG (Turetsky et al, 2014). Regarding N2O, the global emissions estimation from coastal wetlands is up to 4.8 Tg N year−1 and this amount could be further increased due to anthropogenic exacerbation of the N cycle (Murray et al, 2015). CH4 and N2O are two of the most hazardous GHG, both because of their high GW potential (25 and 300 times higher than that of CO2, respectively), and because of their long residence time in the Earth’s atmosphere (12 and 114 years, respectively) (Tangen and Bansal, 2019)
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