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 Saleska, Patrick Crill, William T. Cooper, Jeff P. Chanton, Joel E. Kostka

Research output: Contribution to journalArticle

8 Citations (Scopus)

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 (US)
Pages (from-to)22-32
Number of pages11
JournalOrganic Geochemistry
Volume112
DOIs
StatePublished - Oct 1 2017

Fingerprint

Biological materials
Hydrogenation
decomposition
Decomposition
organic matter
electron
Electrons
Peat
methanogenesis
oxidation
Oxidation
peat
Unsaturated compounds
Quinones
Molecules
Global warming
Carboxylic acids
peatland
food chain
Cellulose

Keywords

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

ASJC Scopus subject areas

  • Geochemistry and Petrology

Cite this

Hydrogenation of organic matter as a terminal electron sink sustains high CO2 : CH4 production ratios during anaerobic decomposition. / Wilson, Rachel M.; Tfaily, Malak M.; Rich, Virginia I; Keller, Jason K.; Bridgham, Scott D.; Zalman, Cassandra Medvedeff; Meredith, Laura; Hanson, Paul J.; Hines, Mark; Pfeifer-Meister, Laurel; Saleska, Scott; Crill, Patrick; Cooper, William T.; Chanton, Jeff P.; Kostka, Joel E.

In: Organic Geochemistry, Vol. 112, 01.10.2017, p. 22-32.

Research output: Contribution to journalArticle

Wilson, RM, Tfaily, MM, Rich, VI, Keller, JK, Bridgham, SD, Zalman, CM, Meredith, L, Hanson, PJ, Hines, M, Pfeifer-Meister, L, Saleska, S, Crill, P, Cooper, WT, Chanton, JP & Kostka, JE 2017, 'Hydrogenation of organic matter as a terminal electron sink sustains high CO2: CH4 production ratios during anaerobic decomposition', Organic Geochemistry, vol. 112, pp. 22-32. https://doi.org/10.1016/j.orggeochem.2017.06.011
Wilson, Rachel M. ; Tfaily, Malak M. ; Rich, Virginia I ; Keller, Jason K. ; Bridgham, Scott D. ; Zalman, Cassandra Medvedeff ; Meredith, Laura ; Hanson, Paul J. ; Hines, Mark ; Pfeifer-Meister, Laurel ; Saleska, Scott ; Crill, Patrick ; Cooper, William T. ; Chanton, Jeff P. ; Kostka, Joel E. / Hydrogenation of organic matter as a terminal electron sink sustains high CO2 : CH4 production ratios during anaerobic decomposition. In: Organic Geochemistry. 2017 ; Vol. 112. pp. 22-32.
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T2 - CH4 production ratios during anaerobic decomposition

AU - Wilson, Rachel M.

AU - Tfaily, Malak M.

AU - Rich, Virginia I

AU - Keller, Jason K.

AU - Bridgham, Scott D.

AU - Zalman, Cassandra Medvedeff

AU - Meredith, Laura

AU - Hanson, Paul J.

AU - Hines, Mark

AU - Pfeifer-Meister, Laurel

AU - Saleska, Scott

AU - Crill, Patrick

AU - Cooper, William T.

AU - Chanton, Jeff P.

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KW - Greenhouse gas

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KW - Peatland

KW - Terminal electron acceptor

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