Thermodynamically controlled preservation of organic carbon in floodplains
Abstract
Organic matter decomposition in soils and terrestrial sediments has a prominent role in the global carbon cycle. Carbon stocks in anoxic environments, such as wetlands and the subsurface of floodplains, are large and presumed to decompose slowly. The degree of microbial respiration in anoxic environments is typically thought to depend on the energetics of available terminal electron acceptors such as nitrate or sulfate; microbes couple the reduction of these compounds to the oxidation of organic carbon. However, it is also possible that the energetics of the organic carbon itself can determine whether it is decomposed. Here we examined water-soluble organic carbon by Fourier-transform ion-cyclotron-resonance mass spectrometry to compare the chemical composition and average nominal oxidation state of carbon-A metric reflecting whether microbial oxidation of organic matter is thermodynamically favourable-in anoxic (sulfidic) and oxic (non-sulfidic) floodplain sediments. We observed distinct minima in the average nominal oxidation state of water-soluble carbon in sediments exhibiting anoxic, sulfate-reducing conditions, suggesting preservation of carbon compounds with nominal oxidation states below the threshold that makes microbial sulfate reduction thermodynamically favourable. We conclude that thermodynamic limitations constitute an important complement to other mechanisms of carbon preservation, such as enzymatic restrictions and mineral association, within anaerobic environments.
- Authors:
-
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource; Stanford Univ., CA (United States). Earth System Science Dept.
- SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Science Lab.
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Climate and Ecosystem Sciences Division
- Stanford Univ., CA (United States). Earth System Science Dept.
- Publication Date:
- Research Org.:
- SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1363868
- Alternate Identifier(s):
- OSTI ID: 1368457; OSTI ID: 1458494
- Grant/Contract Number:
- AC02-76SF00515; FG02-13ER65542; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Geoscience
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 6; Journal ID: ISSN 1752-0894
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 58 GEOSCIENCES; carbon cycle; freshwater ecology
Citation Formats
Boye, Kristin, Noel, Vincent, Tfaily, Malak M., Bone, Sharon E., Williams, Kenneth H., Bargar, John R., and Fendorf, Scott. Thermodynamically controlled preservation of organic carbon in floodplains. United States: N. p., 2017.
Web. doi:10.1038/ngeo2940.
Boye, Kristin, Noel, Vincent, Tfaily, Malak M., Bone, Sharon E., Williams, Kenneth H., Bargar, John R., & Fendorf, Scott. Thermodynamically controlled preservation of organic carbon in floodplains. United States. https://doi.org/10.1038/ngeo2940
Boye, Kristin, Noel, Vincent, Tfaily, Malak M., Bone, Sharon E., Williams, Kenneth H., Bargar, John R., and Fendorf, Scott. Mon .
"Thermodynamically controlled preservation of organic carbon in floodplains". United States. https://doi.org/10.1038/ngeo2940. https://www.osti.gov/servlets/purl/1363868.
@article{osti_1363868,
title = {Thermodynamically controlled preservation of organic carbon in floodplains},
author = {Boye, Kristin and Noel, Vincent and Tfaily, Malak M. and Bone, Sharon E. and Williams, Kenneth H. and Bargar, John R. and Fendorf, Scott},
abstractNote = {Organic matter decomposition in soils and terrestrial sediments has a prominent role in the global carbon cycle. Carbon stocks in anoxic environments, such as wetlands and the subsurface of floodplains, are large and presumed to decompose slowly. The degree of microbial respiration in anoxic environments is typically thought to depend on the energetics of available terminal electron acceptors such as nitrate or sulfate; microbes couple the reduction of these compounds to the oxidation of organic carbon. However, it is also possible that the energetics of the organic carbon itself can determine whether it is decomposed. Here we examined water-soluble organic carbon by Fourier-transform ion-cyclotron-resonance mass spectrometry to compare the chemical composition and average nominal oxidation state of carbon-A metric reflecting whether microbial oxidation of organic matter is thermodynamically favourable-in anoxic (sulfidic) and oxic (non-sulfidic) floodplain sediments. We observed distinct minima in the average nominal oxidation state of water-soluble carbon in sediments exhibiting anoxic, sulfate-reducing conditions, suggesting preservation of carbon compounds with nominal oxidation states below the threshold that makes microbial sulfate reduction thermodynamically favourable. We conclude that thermodynamic limitations constitute an important complement to other mechanisms of carbon preservation, such as enzymatic restrictions and mineral association, within anaerobic environments.},
doi = {10.1038/ngeo2940},
journal = {Nature Geoscience},
number = 6,
volume = 10,
place = {United States},
year = {Mon May 01 00:00:00 EDT 2017},
month = {Mon May 01 00:00:00 EDT 2017}
}
Web of Science
Works referenced in this record:
ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT
journal, June 2005
- Ravel, B.; Newville, M.
- Journal of Synchrotron Radiation, Vol. 12, Issue 4
EXAFS analysis of iron cycling in mangrove sediments downstream a lateritized ultramafic watershed (Vavouto Bay, New Caledonia)
journal, July 2014
- Noël, Vincent; Marchand, Cyril; Juillot, Farid
- Geochimica et Cosmochimica Acta, Vol. 136
Organic carbon distribution, speciation, and elemental correlations within soil microaggregates: Applications of STXM and NEXAFS spectroscopy
journal, November 2007
- Wan, Jiamin; Tyliszczak, Tolek; Tokunaga, Tetsu K.
- Geochimica et Cosmochimica Acta, Vol. 71, Issue 22
Advanced Solvent Based Methods for Molecular Characterization of Soil Organic Matter by High-Resolution Mass Spectrometry
journal, April 2015
- Tfaily, Malak M.; Chu, Rosalie K.; Tolić, Nikola
- Analytical Chemistry, Vol. 87, Issue 10
Mineralization of ancient carbon in the subsurface of riparian forests: ANCIENT RIPARIAN CARBON MINERALIZATION
journal, May 2008
- Gurwick, Noel P.; McCorkle, Daniel M.; Groffman, Peter M.
- Journal of Geophysical Research: Biogeosciences, Vol. 113, Issue G2
Redox zonation: Equilibrium constraints on the Fe(III)/SO4-reduction interface
journal, September 1996
- Postma, Dieke; Jakobsen, Rasmus
- Geochimica et Cosmochimica Acta, Vol. 60, Issue 17
Paradigm shifts in soil organic matter research affect interpretations of aquatic carbon cycling: transcending disciplinary and ecosystem boundaries
journal, January 2014
- Marín-Spiotta, E.; Gruley, K. E.; Crawford, J.
- Biogeochemistry, Vol. 117, Issue 2-3
Automated Analysis of Electrospray Ionization Fourier Transform Ion Cyclotron Resonance Mass Spectra of Natural Organic Matter
journal, July 2006
- Kujawinski, Elizabeth B.; Behn, Mark D.
- Analytical Chemistry, Vol. 78, Issue 13
Riverine flood plains: present state and future trends
journal, September 2002
- Tockner, Klement; Stanford, Jack A.
- Environmental Conservation, Vol. 29, Issue 3
Microbially available carbon in buried riparian soils in a glaciated landscape
journal, January 2008
- Gurwick, Noel P.; Groffman, Peter M.; Yavitt, Joseph B.
- Soil Biology and Biochemistry, Vol. 40, Issue 1
Soil enzymes in a changing environment: Current knowledge and future directions
journal, March 2013
- Burns, Richard G.; DeForest, Jared L.; Marxsen, Jürgen
- Soil Biology and Biochemistry, Vol. 58
Graphical Method for Analysis of Ultrahigh-Resolution Broadband Mass Spectra of Natural Organic Matter, the Van Krevelen Diagram
journal, October 2003
- Kim, Sunghwan; Kramer, Robert W.; Hatcher, Patrick G.
- Analytical Chemistry, Vol. 75, Issue 20
Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules
journal, November 2007
- Lorenz, Klaus; Lal, Rattan; Preston, Caroline M.
- Geoderma, Vol. 142, Issue 1-2
Physico-Chemical Heterogeneity of Organic-Rich Sediments in the Rifle Aquifer, CO: Impact on Uranium Biogeochemistry
journal, December 2015
- Janot, Noémie; Lezama Pacheco, Juan S.; Pham, Don Q.
- Environmental Science & Technology, Vol. 50, Issue 1
Characterization of dissolved organic matter in Lake Superior and its watershed using ultrahigh resolution mass spectrometry
journal, February 2012
- Minor, Elizabeth C.; Steinbring, Carla J.; Longnecker, Krista
- Organic Geochemistry, Vol. 43
Soil burial contributes to deep soil organic carbon storage
journal, February 2014
- Chaopricha, Nina T.; Marín-Spiotta, Erika
- Soil Biology and Biochemistry, Vol. 69
Distribution and Characteristics of Dissolved Organic Matter in Mangrove Sediment Pore Waters along the Coastline of French Guiana
journal, July 2006
- Marchand, C.; Albéric, P.; Lallier-Vergès, E.
- Biogeochemistry, Vol. 81, Issue 1
Carbon (1s) NEXAFS Spectroscopy of Biogeochemically Relevant Reference Organic Compounds
journal, January 2009
- Solomon, Dawit; Lehmann, Johannes; Kinyangi, James
- Soil Science Society of America Journal, Vol. 73, Issue 6
From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter
journal, February 2006
- Koch, B. P.; Dittmar, T.
- Rapid Communications in Mass Spectrometry, Vol. 20, Issue 5
Biogeochemistry of dissolved organic matter in an anoxic intertidal creek bank
journal, September 2014
- Seidel, Michael; Beck, Melanie; Riedel, Thomas
- Geochimica et Cosmochimica Acta, Vol. 140
Changes in peat chemistry associated with permafrost thaw increase greenhouse gas production
journal, April 2014
- Hodgkins, S. B.; Tfaily, M. M.; McCalley, C. K.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 16
Are oxygen limitations under recognized regulators of organic carbon turnover in upland soils?
journal, January 2016
- Keiluweit, Marco; Nico, Peter S.; Kleber, Markus
- Biogeochemistry, Vol. 127, Issue 2-3
The retention of organic matter in soils
journal, February 1988
- Oades, J. M.
- Biogeochemistry, Vol. 5, Issue 1
XAS Evidence of As(V) Association with Iron Oxyhydroxides in a Contaminated Soil at a Former Arsenical Pesticide Processing Plant
journal, December 2005
- Cancès, B.; Juillot, F.; Morin, G.
- Environmental Science & Technology, Vol. 39, Issue 24
C 1s K-edge near edge X-ray absorption fine structure (NEXAFS) spectroscopy for characterizing functional group chemistry of black carbon
journal, October 2011
- Heymann, Karen; Lehmann, Johannes; Solomon, Dawit
- Organic Geochemistry, Vol. 42, Issue 9
Hailstones: A Window into the Microbial and Chemical Inventory of a Storm Cloud
journal, January 2013
- Šantl-Temkiv, Tina; Finster, Kai; Dittmar, Thorsten
- PLoS ONE, Vol. 8, Issue 1
How do long-term development and periodical changes of river–floodplain systems affect the fate of contaminants? Results from European rivers
journal, December 2009
- Lair, G. J.; Zehetner, F.; Fiebig, M.
- Environmental Pollution, Vol. 157, Issue 12
Persistence of soil organic matter as an ecosystem property
journal, October 2011
- Schmidt, Michael W. I.; Torn, Margaret S.; Abiven, Samuel
- Nature, Vol. 478, Issue 7367
A conceptual model of organo-mineral interactions in soils: self-assembly of organic molecular fragments into zonal structures on mineral surfaces
journal, June 2007
- Kleber, M.; Sollins, P.; Sutton, R.
- Biogeochemistry, Vol. 85, Issue 1
The molecularly-uncharacterized component of nonliving organic matter in natural environments
journal, October 2000
- Hedges, J. I.; Eglinton, G.; Hatcher, P. G.
- Organic Geochemistry, Vol. 31, Issue 10
Role of proteins in soil carbon and nitrogen storage: controls on persistence
journal, March 2007
- Rillig, Matthias C.; Caldwell, Bruce A.; Wösten, Han A. B.
- Biogeochemistry, Vol. 85, Issue 1
Legacy of human-induced C erosion and burial on soil-atmosphere C exchange
journal, November 2012
- Van Oost, K.; Verstraeten, G.; Doetterl, S.
- Proceedings of the National Academy of Sciences, Vol. 109, Issue 47
Illuminated darkness: Molecular signatures of Congo River dissolved organic matter and its photochemical alteration as revealed by ultrahigh precision mass spectrometry
journal, May 2010
- Stubbins, Aron; Spencer, Robert G. M.; Chen, Hongmei
- Limnology and Oceanography, Vol. 55, Issue 4
Predicting the rate of microbial respiration in geochemical environments
journal, March 2005
- Jin, Qusheng; Bethke, Craig M.
- Geochimica et Cosmochimica Acta, Vol. 69, Issue 5
Sulfur Speciation in Soil by S K -Edge XANES Spectroscopy: Comparison of Spectral Deconvolution and Linear Combination Fitting
journal, April 2011
- Prietzel, Jörg; Botzaki, Anna; Tyufekchieva, Nora
- Environmental Science & Technology, Vol. 45, Issue 7
Spatial Distribution of Carbon in the Subsurface of Riparian Zones
journal, January 2009
- Blazejewski, Gary A.; Stolt, Mark H.; Gold, Arthur J.
- Soil Science Society of America Journal, Vol. 73, Issue 5
Soil Organic Carbon Stocks in a Large Eutrophic Floodplain Forest of the Southeastern Atlantic Coastal Plain, USA
journal, January 2015
- Ricker, Matthew C.; Lockaby, B. Graeme
- Wetlands, Vol. 35, Issue 2
Organic carbon and sulphur compounds in wetland soils: insights on structure and transformation processes using K-edge XANES and NMR spectroscopy
journal, July 2003
- Jokic, Aleksander; Cutler, Jeffrey N.; Ponomarenko, Elena
- Geochimica et Cosmochimica Acta, Vol. 67, Issue 14
Early oxidation of organic matter in pelagic sediments of the eastern equatorial Atlantic: suboxic diagenesis
journal, July 1979
- Froelich, P. N.; Klinkhammer, G. P.; Bender, M. L.
- Geochimica et Cosmochimica Acta, Vol. 43, Issue 7
Degradation of natural organic matter: A thermodynamic analysis
journal, April 2011
- LaRowe, Douglas E.; Van Cappellen, Philippe
- Geochimica et Cosmochimica Acta, Vol. 75, Issue 8
Deep soil organic matter—a key but poorly understood component of terrestrial C cycle
journal, May 2010
- Rumpel, Cornelia; Kögel-Knabner, Ingrid
- Plant and Soil, Vol. 338, Issue 1-2
From mass to structure: an aromaticity index for high-resolution mass data of natural organic matter
journal, December 2015
- Koch, B. P.; Dittmar, T.
- Rapid Communications in Mass Spectrometry, Vol. 30, Issue 1
C 1s K-edge near edge X-ray absorption fine structure (NEXAFS) spectroscopy for characterizing functional group chemistry of black carbon
text, January 2011
- Heymann, K.; Lehmann, Johannes; Solomon, D.
- Elsevier
Persistence of soil organic matter as an ecosystem property
text, January 2011
- Schmidt, M. W. I.; Torn, M. S.; Abiven, S.
- Nature Publishing Group
Bacterial Metabolism
journal, June 1947
- Woods, D. D.
- Annual Review of Biochemistry, Vol. 16, Issue 1
Works referencing / citing this record:
Pulse of dissolved organic matter alters reciprocal carbon subsidies between autotrophs and bacteria in stream food webs
journal, January 2020
- Demars, Benoît O. L.; Friberg, Nikolai; Thornton, Barry
- Ecological Monographs, Vol. 90, Issue 1
High variability in iron-bound organic carbon among five boreal lake sediments
journal, May 2018
- Peter, Simone; Sobek, Sebastian
- Biogeochemistry, Vol. 139, Issue 1
Hydrogeomorphic controls on soil carbon composition in two classes of subalpine wetlands
journal, September 2019
- Daugherty, Ellen E.; McKee, Georgina A.; Bergstrom, Robert
- Biogeochemistry, Vol. 145, Issue 1-2
Elevated moisture stimulates carbon loss from mineral soils by releasing protected organic matter
journal, November 2017
- Huang, Wenjuan; Hall, Steven J.
- Nature Communications, Vol. 8, Issue 1
River channel connectivity shifts metabolite composition and dissolved organic matter chemistry
journal, January 2019
- Lynch, Laurel M.; Sutfin, Nicholas A.; Fegel, Timothy S.
- Nature Communications, Vol. 10, Issue 1
Persistent organic matter in oxic subseafloor sediment
journal, January 2019
- Estes, Emily R.; Pockalny, Robert; D’Hondt, Steven
- Nature Geoscience, Vol. 12, Issue 2
Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer
journal, July 2017
- Pan, Donald; Nolan, Jason; Williams, Kenneth H.
- Frontiers in Microbiology, Vol. 8
Changes in Carbon Oxidation State of Metagenomes Along Geochemical Redox Gradients
journal, February 2019
- Dick, Jeffrey M.; Yu, Miao; Tan, Jingqiang
- Frontiers in Microbiology, Vol. 10
Composition-Dependent Sorptive Fractionation of Anthropogenic Dissolved Organic Matter by Fe(III)-Montmorillonite
journal, March 2018
- Young, Robert; Avneri-Katz, Shani; McKenna, Amy
- Soil Systems, Vol. 2, Issue 1
Molecular characterization of organic matter mobilized from Bangladeshi aquifer sediment: tracking carbon compositional change during microbial utilization
journal, January 2018
- Pracht, Lara E.; Tfaily, Malak M.; Ardissono, Robert J.
- Biogeosciences, Vol. 15, Issue 6
Shifting mineral and redox controls on carbon cycling in seasonally flooded mineral soils
journal, January 2019
- LaCroix, Rachelle E.; Tfaily, Malak M.; McCreight, Menli
- Biogeosciences, Vol. 16, Issue 13
Spatial gradients in the characteristics of soil-carbon fractions are associated with abiotic features but not microbial communities
journal, January 2019
- Sengupta, Aditi; Indivero, Julia; Gunn, Cailene
- Biogeosciences, Vol. 16, Issue 19
Modeling anaerobic soil organic carbon decomposition in Arctic polygon tundra: insights into soil geochemical influences on carbon mineralization
journal, January 2019
- Zheng, Jianqiu; Thornton, Peter E.; Painter, Scott L.
- Biogeosciences, Vol. 16, Issue 3
Co-located contemporaneous mapping of morphological, hydrological, chemical, and biological conditions in a 5th-order mountain stream network, Oregon, USA
journal, January 2019
- Ward, Adam S.; Zarnetske, Jay P.; Baranov, Viktor
- Earth System Science Data, Vol. 11, Issue 4
Geomorphic regulation of floodplain soil organic carbon concentration in watersheds of the Rocky and Cascade Mountains, USA
journal, January 2018
- Scott, Daniel N.; Wohl, Ellen E.
- Earth Surface Dynamics, Vol. 6, Issue 4
Molecular characterization of organic matter mobilized from Bangladeshi aquifer sediment: tracking carbon compositional change during microbial utilization
posted_content, July 2017
- Pracht, Lara E.; Tfaily, Malak M.; Ardissono, Robert J.
- Biogeosciences Discussions
Co-located contemporaneous mapping of morphological, hydrological, chemical, and biological conditions in a 5th-order mountain stream network, Oregon, USA
text, January 2019
- Ward, Adam S.; Zarnetske, Jay P.; Baranov, Viktor
- ETH Zurich
Elevated moisture stimulates carbon loss from mineral soils by releasing protected organic matter
journal, November 2017
- Huang, Wenjuan; Hall, Steven J.
- Nature Communications, Vol. 8, Issue 1
River channel connectivity shifts metabolite composition and dissolved organic matter chemistry
journal, January 2019
- Lynch, Laurel M.; Sutfin, Nicholas A.; Fegel, Timothy S.
- Nature Communications, Vol. 10, Issue 1
Abundance and Distribution of Microbial Cells and Viruses in an Alluvial Aquifer
journal, July 2017
- Pan, Donald; Nolan, Jason; Williams, Kenneth H.
- Frontiers in Microbiology, Vol. 8
Changes in Carbon Oxidation State of Metagenomes Along Geochemical Redox Gradients
journal, February 2019
- Dick, Jeffrey M.; Yu, Miao; Tan, Jingqiang
- Frontiers in Microbiology, Vol. 10