Principal Investigators

Ian Bourg
Amilcare Porporato
Howard A. Stone
Xinning Zhang

At a Glance

The objective of this project is to understand a key control on the stability of soil carbon: its protection by fine-grained minerals. Field experiments suggest that roughly half of the organic carbon present in soils is protected from microbial respiration by certain fine-grained minerals, but the mechanism of this mineral protection remains unknown. The Bourg, Porporato, Stone, and Zhang groups are using a unique combination of experimental and simulation approaches, spanning spatial scales ranging from molecules to landscapes, to elucidate this mechanism. These results will enable more accurate Earth System Model predictions of soil carbon dynamics and inform practical strategies for enhancing the soil carbon sink

 

Research Highlight

Soils are the largest pool of carbon near the Earth’s surface, roughly as large as the atmosphere, biosphere, and surface ocean combined. Each year, soils take up about 61 GtC (gigatons of carbon), primarily as plant residues and root exudates, while emitting about 59 GtC of carbon, primarily as microbial carbon dioxide (CO2) and methane (CH4) (Lehmann & Kleber, 2015). Because of the imbalance between soil carbon uptake and emissions, soils presently act as a net carbon sink that absorbs about 2 GtC per year (~20% of anthropogenic CO2 emissions). This carbon sink is sensitive to changes in temperature, rainfall, and soil management, but a detailed predictive understanding of its magnitude and evolution remains elusive (Sulman et al., 2014; Hicks Pries et al., 2017; Mayer et al., 2018).

Recent meta-analyses of field-scale data reveal that a key predictor of soil carbon storage is the abundance of certain fine-grained minerals, in particular, smectite clay minerals in temperate soils and Fe and Al oxides in tropical and boreal rainforest soils (Rasmussen et al., 2018). A primary goal of this project is to decipher the fundamental mechanisms that cause this correlation in order to inform new soil carbon sequestration approaches. The mechanism likely involves couplings between soil microbiology, clay surface geochemistry, and the hydrologic cycle at various spatial and temporal scales that remain largely unexplored. Progress towards this goal is enabled by a unique combination of field-scale models (Porporato), microfluidic experiments (Stone), microbial ecology techniques (Zhang), and atomistic simulations (Bourg), which are detailed below

The Porporato Group is developing field-scale models of the evolution of soil hydrology, microbiology, and geochemistry. The models consist of ordinary differential equations governing the time evolution of the mass of different species in different soil layers. The processes are modeled through specific kinetic laws calibrated through data from laboratory experiments and field observations. This effort is enhanced by the Porporato group’s access to unique datasets of laboratory and field measurements (Barcellos et al., 2018) through the network of long-term field experiments of the National Science Foundation- funded Critical Zone Observatories. The research focuses particularly on understanding, first, how the formation and transport dynamics of soil clays are coupled to soil hydrology and carbon decomposition and, second, how the redox cycling of iron is used in microbial carbon decomposition in humid tropical soils that experience frequent fluctuations in soil O2. The second topic is also relevant to CMI efforts on CH4, as illustrated by preliminary estimates from field sites in Puerto Rico showing that Fe cycling can strongly inhibit the microbial production of CH4 in tropical soils (Hall et al., 2013).

A key breakthrough in 2018 was the development of a model that captures the interaction between the hydrologic cycle and the pace of soil biogeochemical processes, in particular, the formation and transport of clays and the Fe-cycle (Calabrese et al., 2018; Calabrese & Porporato, 2018). Preliminary results shown in Figure 6.1 illustrate the ability of the clay transport model to predict the clay distribution profile. This profile originates from the balance between clay leaching from water percolation events and surface erosion processes, which tend to remove clay particles from above. The figure also illustrates how the time evolution of dissolved Fe2+, which results from the reductive dissolution of Fe3+ and associated carbon decompositions, is controlled by daily soil moisture fluctuations in a tropic soil.

Environment map
Figure 6.1. (a) Soil clay content with depth (% weight of total clay) from texture measurements (red points) collected at the Calhoun Critical Zone Observatory, South Carolina, and from the model of clay translocation (solid line). The dashed line represents the estimated residence time of clays. (b) Time evolution of modeled soil moisture (top) and dissolved Fe2+ (bottom) for soils at the Bisley Watershed in Luquillo Experimental Forest, Puerto Rico. The model was parameterized with laboratory experiments conducted on soil samples from the field site.

The Stone group is applying its expertise in microfluidic technology to obtain direct evidence on how bacterial growth (current experiments utilize Pseudomonas aeruginosa) and activity are affected by clay minerals and aggregates. Preliminary results suggest an intriguing potential new mechanism, whereby the slowdown of soil carbon decomposition by clay may be caused by the clay-induced flocculation (clumping) and sedimentation of bacteria (perhaps because this flocculation may inhibit the transport of bacteria through porous soil). Preliminary experiments (Figure 6.2) and confocal microscopy observations support the hypothesis that clay minerals may induce bacterial flocculation and sedimentation. Future microfluidic experiments will involve tracking bacterial transport and growth in model soils with and without clay, and so will provide direct evidence to test the current soil-carbon-clay interaction hypothesis. Initial steps in the research have benefitted from frequent discussions with the Bourg and Zhang groups.

Bacteria Settling Map and imge
Figure 6.2. (Left) Evolution of optical density, which is proportional to bacterial cell density in the solution containing bacteria, Pseudomonas aeruginosa, with clay (circles) and without clay (crosses). (Right) Aggregation of bacteria in culture solution with clay particles, shown as bright red dots in the middle of the image. Scale bar: 25 microns.

The Zhang group uses microbial ecology, physiology, and biogeochemical measurement approaches to study the relationship between the production greenhouse gases such as CH4 and CO2, microbial communities, and reactive metal minerals in hydrologically dynamic, carbon-rich environments like wetlands. This work, funded by the CMI Methane project, is highly complementary to ongoing research in the Stone, Porporato, and Bourg groups, as it provides a contrasting view on carbon cycling in clay- poor environments to enable a full understanding of interactions between microbes, minerals, carbon, and water. An exciting discovery in 2018 was the identification of a metal-based, potentially new abiotic mechanism for CH4 production in wetlands. In addition to research on wetland methane (further outlined in the Methane portion of this CMI annual report), the Zhang group works closely with the Stone group to support their experimental investigations.

The Bourg group is using all-atom molecular dynamics (MD) simulations to gain fundamental insight into mineral-organic association. The simulations use the supercomputers of the U.S. Department of Energy to solve Newton’s equations of motion for mineral-water-organic systems of about 105 atoms using semi-empirical models of all relevant interatomic interactions. The research focuses particularly on understanding, first, how organic molecules interact with mineral surfaces and, second, how organic molecules influence the wettability of mineral surfaces by water versus non-aqueous fluids (e.g., air or CO2).

A key breakthrough in 2018 was the development and validation of an MD simulation methodology that accurately predicts the affinity of organic molecules for smectite clay surfaces (Willemsen et al., 2018).

Specifically, simulations and supporting experiments examined the adsorption of 10 different organic molecules with a range of molecular weights and hydrophilicities (phthalate esters, polycyclic aromatic hydrocarbons, and perfluorinated alkyl substances) on a stack of two smectite clay nanoparticles. Results showed that organic molecules consistently have a strong affinity for the clay surfaces (Figure 6.3). Contrary to the predominant theory of soil carbon protection by mineral surfaces, this affinity is primarily entropic, i.e., the tendency of soil carbon to become associated with mineral surfaces is determined by hydrophobicity rather than by the interaction of specific functional groups with the mineral surface.

Molecular Dynamics Simulation map
Figure 6.3. (Top) Snapshot of a simulation cell containing two smectite clay nanoparticles (1 nm thick particles with 0.6 nm thick interlayer nanopores) in contact with bulk-liquid-like water (0.1 M CaCl2 solution). The clay structure is shown as red, yellow, and orange polyhedra (SiO4, AlO6, and MgO6, respectively); water molecules are shown as small blue dots; electrolyte ions (Ca, Cl) are shown as purple and green spheres; adsorbed organic molecules (in this case, phthalate esters) are shown as pink, blue, and white spheres. (Bottom) Molecular dynamics simulation reconstruction of the contributions of enthalpic interactions (i.e., attraction of specific organic moieties to the mineral surface) and entropic interactions (predominantly water’s tendency to expel hydrophobic solutes) to the overall free energy of adsorption are reported as blue diamonds and yellow circles for six phthalate esters with various shapes and sizes. Greater negative free energies of adsorption indicate greater affinity for the mineral surface.

Another important breakthrough in 2018 was the demonstration that MD simulations can predict details of the wettability of mineral surfaces by water versus non-aqueous fluids that are challenging to resolve using experiments (Sun and Bourg, 2018). In particular, MD simulations were used to predict the influence of organic matter and multiphase flow dynamics on water imbibition and drainage in small pores in the presence of supercritical CO2 (Figure 6.4). The results have implications for understanding the coupled fluxes of water and carbon in soils, but also broader implications for predicting the flow of water and CO2 in geologic formations during carbon capture and storage and CO2-enhanced oil recovery.

Snapshot of a simulation cell containing water
Figure 6.4. Snapshot of a simulation cell containing water (blue sticks), CO2 (gray spheres), and decanoic acid molecules (green spheres) between two parallel quartz surfaces. The simulations predict the existence of a stable adsorbed water film on the quartz surfaces and a water meniscus bridging the two quartz surfaces. Calculation of the local stresses (not shown) reveals that the capillary pressure difference between the two fluids is consistent with macroscopic-scale theories (i.e., the Young-Laplace equation). In the system shown in the figure, a uniform force fx applied to the fluid atoms drives fluid flow from left to right. As a result, the organic molecules accumulate at the trailing edge of the CO2 bubble (left insert) and the adsorbed water film thickness decreases with distance from the leading edge of the bubble (lower inserts).

References

Hall, S.J., W.H. McDowell, and W.L. Silver, 2013. When wet gets wetter: decoupling of moisture, redox biogeochemistry, and greenhouse gas fluxes in a humid tropical forest soil. Ecosystems, 16: 576. doi. org/10.1007/s10021-012-9631-2.

Hicks Pries, C.E., C. Castanha, R. Porras, and M.S. Torn, 2017. The whole-soil carbon flux in response to warming. Science 355: 1420. doi.org/10.1126/science.aal1319.

Lehmann, J., and M. Kleber, 2015. The contentious nature of soil organic matter. Nature, 528, 60. doi. org/10.1038/nature16069.

Mayer, A., Z. Hausfather, A.D. Jones, and W.L. Silver, 2018. The potential of agricultural land management to contribute to lower global surface temperature. Science Advances 4: eaaq0932. doi.org/10.1126/sciadv. aaq0932.

Rasmussen, C. et al., 2018. Beyond clay: towards an improved set of variables for predicting soil organic matter content. Biogeochemistry 137: 297. doi.org/10.1007/s10533-018-0424-3.

Sulman, B.N., R.P. Phillips, A.C. Oishi, E. Shevliakova, and S.W. Pacala, 2014. Microbe-driven turnover offsets mineral-mediated storage of soil carbon under elevated CO2. Nature Climate Change 4:1099. doi. org/10.1038/NCLIMATE2436.