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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 CO 2 and CH 4 for each molecule of organic matter degraded. However, CO 2:CH 4 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 CO 2 has an oxidation state of +4, if CH 4 (oxidation state -4) is not produced in equal ratio, then some other compound(s) must balance CO 2 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 CO 2:CH 4 >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 asmore » 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. In conclusion, this mechanism for CO 2 generation without concomitant CH 4 production has the potential to regulate the global warming potential of peatlands by elevating CO 2:CH 4 production ratios.« less

Authors:
 [1];  [2];  [3];  [4];  [5];  [4];  [6]; ORCiD logo [7];  [8];  [5];  [6];  [9];  [10];  [1];  [11]
  1. Florida State Univ., Tallahassee, FL (United States). Dept. of Earth Ocean and Atmospheric Sciences
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  3. The Ohio State Univ., Columbus, OH (United States). Dept of Microbiology
  4. Chapman Univ., Orange, CA (United States). Schmid College of Science and Technology
  5. Univ. of Oregon, Eugene, OR (United States). Inst. of Ecology and Evolution
  6. Univ. of Arizona, Tucson, AZ (United States). Dept. of Ecology and Evolutionary Biology
  7. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  8. Univ. of Massachusetts, Lowell, MA (United States). Dept. of Biological Sciences
  9. Stockholm Univ. (Sweden). Dept. of Geological Sciences
  10. Florida State Univ., Tallahassee, FL (United States). Dept. of Chemistry and Biochemistry
  11. Georgia Inst. of Technology, Atlanta, GA (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1368410
Alternate Identifier(s):
OSTI ID: 1471954
Grant/Contract Number:  
AC05-76RL01830; AC05-00OR22725; SC0004632; SC0010580; SC0012088; SC0014416
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Organic Geochemistry
Additional Journal Information:
Journal Volume: 112; Journal ID: ISSN 0146-6380
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; anaerobic methanogenesis; C cycle; greenhouse gas; terminal electron acceptor; peatland; microbial respiration

Citation Formats

Wilson, Rachel M., Tfaily, Malak M., Rich, Virginia I., Keller, Jason K., Bridgham, Scott D., Medvedeff Zalman, Cassandra, 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 CO2 :CH4 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., Medvedeff Zalman, Cassandra, 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 CO2 :CH4 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., Medvedeff Zalman, Cassandra, 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.. Mon . "Hydrogenation of Organic Matter as a Terminal Electron Sink Sustains High CO2 :CH4 Production Ratios During Anaerobic Decomposition". United States. doi:10.1016/j.orggeochem.2017.06.011. https://www.osti.gov/servlets/purl/1368410.
@article{osti_1368410,
title = {Hydrogenation of Organic Matter as a Terminal Electron Sink Sustains High CO2 :CH4 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 Medvedeff Zalman, Cassandra 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. In conclusion, 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 = ,
volume = 112,
place = {United States},
year = {Mon Jul 03 00:00:00 EDT 2017},
month = {Mon Jul 03 00:00:00 EDT 2017}
}

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