Hydrogenation of organic matter as a terminal electron sink sustains high CO2:CH4 production ratios during anaerobic decomposition

Rachel M. Wilson, Malak M. Tfaily, Virginia I. Rich, Jason K. Keller, Scott D. Bridgham, Cassandra Medvedeff Zalman, Laura Meredith, Paul J. Hanson, Mark Hines, Laurel Pfeifer-Meister, Scott R. Saleska, Patrick Crill, William T. Cooper, Jeff P. Chanton, Joel E. Kostka

Research output: Contribution to journalArticlepeer-review

45 Scopus citations

Abstract

Once inorganic electron acceptors are depleted, organic matter in anoxic environments decomposes by hydrolysis, fermentation, and methanogenesis, requiring syntrophic interactions between microorganisms to achieve energetic favorability. In this classic anaerobic food chain, methanogenesis represents the terminal electron accepting (TEA) process, ultimately producing equimolar CO2 and CH4 for each molecule of organic matter degraded. However, CO2:CH4 production in Sphagnum-derived, mineral-poor, cellulosic peat often substantially exceeds this 1:1 ratio, even in the absence of measureable inorganic TEAs. Since the oxidation state of C in both cellulose-derived organic matter and acetate is 0, and CO2 has an oxidation state of +4, if CH4 (oxidation state −4) is not produced in equal ratio, then some other compound(s) must balance CO2 production by receiving 4 electrons. Here we present evidence for ubiquitous hydrogenation of diverse unsaturated compounds that appear to serve as organic TEAs in peat, thereby providing the necessary electron balance to sustain CO2:CH4 > 1. While organic electron acceptors have previously been proposed to drive microbial respiration of organic matter through the reversible reduction of quinone moieties, the hydrogenation mechanism that we propose, by contrast, reduces C–C double bonds in organic matter thereby serving as (1) a terminal electron sink, (2) a mechanism for degrading complex unsaturated organic molecules, (3) a potential mechanism to regenerate electron-accepting quinones, and, in some cases, (4) a means to alleviate the toxicity of unsaturated aromatic acids. This mechanism for CO2 generation without concomitant CH4 production has the potential to regulate the global warming potential of peatlands by elevating CO2:CH4 production ratios.

Original languageEnglish
Pages (from-to)22-32
Number of pages11
JournalOrganic Geochemistry
Volume112
DOIs
StatePublished - Oct 2017

Funding

This material is based upon work supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the U.S. Department of Energy under contract DE-AC05-00OR22725. Work in Sweden was funded by the US Department of Energy Office of Biological and Environmental Research under the Genomic Science program (Awards DE-SC0004632 and DESC0010580). Work in Minnesota was supported by the Terrestrial Ecosystem Science (TES) Program, under U.S. Department of Energy contracts # DE-SC0012088 and DE-SC0014416. We’d like to thank the Environmental Molecular Sciences Laboratory at Pacific Northwest National Laboratory (Richland, WA) for access to their 12T FTICRMS and for support to MM Tfaily. We thank the Abisko Scientific Research Station for sampling infrastructure and Kelsey Crossen for assistance with the microbial data from Sweden. SR Saleska and VI Rich received support through the Ecosystem Genomics Initiative, by the University of Arizona Technology and Research Initiative Fund, through the Water, Environmental and Energy Solutions Initiative. This work was supported by the U.S. Department of Energy , Office of Science , Office of Biological and Environmental Research [Grants: DE-AC05-00OR22725 , DE-SC0004632 , DESC0010580 , DE-SC0012088 and DE-SC0014416 ].

Keywords

  • Anaerobic methanogenesis
  • C cycle
  • Greenhouse gas
  • Microbial respiration
  • Peatland
  • Terminal electron acceptor

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