skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Hydrogenation of organic matter as a terminal electron sink sustains high CO 2 :CH 4 production ratios during anaerobic decomposition

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 formore » 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.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1406779
Report Number(s):
PNNL-SA-127483
Journal ID: ISSN 0146-6380; 49279; 48467; 49521; KP1704020
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Organic Geochemistry; Journal Volume: 112; Journal Issue: C
Country of Publication:
United States
Language:
English
Subject:
58 GEOSCIENCES; Environmental Molecular Sciences Laboratory

Citation Formats

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 R., Crill, Patrick, Cooper, William T., Chanton, Jeff P., and Kostka, Joel E. Hydrogenation of organic matter as a terminal electron sink sustains high CO 2 :CH 4 production ratios during anaerobic decomposition. United States: N. p., 2017. Web. doi: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 R., Crill, Patrick, Cooper, William T., Chanton, Jeff P., & Kostka, Joel E. Hydrogenation of organic matter as a terminal electron sink sustains high CO 2 :CH 4 production ratios during anaerobic decomposition. United States. doi: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 R., Crill, Patrick, Cooper, William T., Chanton, Jeff P., and Kostka, Joel E. Sun . "Hydrogenation of organic matter as a terminal electron sink sustains high CO 2 :CH 4 production ratios during anaerobic decomposition". United States. doi:10.1016/j.orggeochem.2017.06.011.
@article{osti_1406779,
title = {Hydrogenation of organic matter as a terminal electron sink sustains high CO 2 :CH 4 production ratios during anaerobic decomposition},
author = {Wilson, Rachel M. and Tfaily, Malak M. and Rich, Virginia I. and Keller, Jason K. and Bridgham, Scott D. and Zalman, Cassandra Medvedeff and Meredith, Laura and Hanson, Paul J. and Hines, Mark and Pfeifer-Meister, Laurel and Saleska, Scott R. and Crill, Patrick and Cooper, William T. and Chanton, Jeff P. and Kostka, Joel E.},
abstractNote = {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.},
doi = {10.1016/j.orggeochem.2017.06.011},
journal = {Organic Geochemistry},
number = C,
volume = 112,
place = {United States},
year = {Sun Oct 01 00:00:00 EDT 2017},
month = {Sun Oct 01 00:00:00 EDT 2017}
}