Novel mechanism shifts understanding of the reactivity of carbon in subsurface stocks.
A new study provides important insights into why carbon persists in waterlogged soil and subsurface sediments. Energetic constraints prevent microbial respiration of certain organic carbon compounds, leaving a pool of water-soluble carbon that is susceptible to oxidation or export and subsequent decomposition in downstream, aerated environments.
Terrestrial, anoxic environments hold large stocks of carbon, and knowledge of the dynamics of these stocks is insufficient. Thermodynamic limitations on organic carbon decomposition operate differently than better-recognized kinetic and spatial constraints, and this must be accounted for in models predicting carbon cycling rates. The new findings imply that organic carbon stocks respond differently than previously thought to changes in sediment water saturation. Moreover, carbon exported from anoxic environments has the potential to drive nutrient, contaminant, and carbon cycles in downstream aquatic ecosystems. The study also demonstrates the benefits of combining X-ray absorption spectroscopy (XAS) at the Stanford Synchrotron Radiation Lightscource (SSRL) with Fourier transform ion cyclotron resonance mass spectrometry (FT-ICR-MS) at the Environmental Molecular Sciences Laboratory (EMSL).
It is well recognized that carbon persists in environments where the oxygen levels are low. Carbon stocks existing in floodplains, wetlands, and subsurface sediments, which often are suboxic to anoxic, comprise a considerable portion of the global dynamic carbon inventory. In spite of the importance to accurately represent the dynamics of these carbon stocks in global, regional, and local carbon models, the mechanisms responsible for carbon preservation in anoxic conditions are unclear. The degradation of organic matter takes place through multiple steps, involving enzymatic and metabolic processes carried out by many different types of microorganisms. However, the last step, the oxidation of organic molecules to carbon dioxide through microbial respiration, requires the molecules to be water-soluble and small enough to enter the microbial cell. In addition to this, the oxidation of carbon must generate enough energy to support microbial growth. With oxygen present the respiratory oxidation of any carbon compound is thermodynamically viable; it provides sufficient energy to sustain growth. But without oxygen, some carbon compounds, mostly belonging to the chemical classes of lipids and proteins, become thermodynamically unviable for oxidation, in spite of being dissolved and small enough to enter the microbial cell. This changes the chemical composition of the water-soluble carbon in environments where this thermodynamic preservation mechanism is operational.
In a Stanford University and SSRL-based study, Boye et al. (2017), utilized the shift in water soluble–carbon chemistry to demonstrate the relevance of thermodynamic limitations for preserving carbon in field samples from anoxic floodplain sediments from four sites across the upper Colorado River Basin. X-ray absorption spectroscopy at SSRL was used to identify sediments containing sulfides produced by microbial respiration in the absence of oxygen. The water-soluble carbon from these sediments was then analyzed by FT-ICR-MS at EMSL and compared to that from oxic sediment samples. The results reveal a clear difference in carbon chemistry consistent with theoretically calculated thermodynamic thresholds and provide unprecedented field-based evidence for thermodynamic preservation of carbon in anoxic conditions. This is important because it illuminates a mechanism previously unrepresented in carbon cycling models and further highlights that water-soluble, and thus readily exported, carbon from anoxic environments is highly susceptible to rapid decomposition upon exposure to oxygen. The downstream implications of this reactive carbon source are currently not fully understood, but are likely substantial.
BER Program Manager
DOE Office of Biological and Environmental Research, Climate and Environmental Sciences Division
Earth System Science, Stanford University
SLAC National Accelerator Laboratory, Stanford Synchrotron Radiation Lightsource
Funding was provided by the Subsurface Biogeochemistry Research (SBR) program of the Office of Biological and Environmental Research (BER), within the U.S. Department of Energy (DOE) Office of Science, to the SLAC Scientific Focus Area (SFA) under contract DE-AC02-76SF00515 to SLAC and to Scott Fendorf through BER's Terrestrial Ecosystem Science (TES) program under Award Number DE-FG02-13ER65542. Use of the Stanford Synchrotron Radiation Lightsource (SSRL) is supported by the Office of Basic Energy Sciences, within the DOE Office of Science. A portion of the research was conducted at the Environmental Molecular Sciences Laboratory (EMSL), a DOE Office of Science user facility sponsored by BER and located at Pacific Northwest National Laboratory. Field operations were supported through Lawrence Berkeley National Laboratory’s Sustainable Systems SFA (DOE BER, contract DE-AC02-05CH11231) and through the DOE Office of Legacy Management (DOE-LM). Research described in this paper was performed at beamline 11ID-1 at the Canadian Light Source (CLS), which is supported by the following Canadian entities: Natural Sciences and Engineering Research Council of Canada (NSERC), Canadian Institutes of Health Research (CIHR), National Research Council (NRC), Western Economic Development Canada (WEDC), the University of Saskatchewan, and the Province of Saskatchewan.
Boye, K., Noël, V., Tfaily, M. M., Bone, S.E., Williams, K. H., Bargar, J. R., and Fendorf, S. “Thermodynamically controlled preservation of organic carbon in floodplains,” Nature Geoscience 10, 415–19 (2017). [DOI:10.1038/ngeo2940].
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