4D imaging reveals mechanisms of clay-carbon protection and release
Authors: Judy Q. Yang, Xinning Zhang, Ian C. Bourg & Howard A. StoneNature Communications volume 12, Article number: 622 (2021)
Abstract
Soil absorbs about 20% of anthropogenic carbon emissions annually, and clay is one of the key carbon-capture materials. Although sorption to clay is widely assumed to strongly retard the microbial decomposition of soil organic matter, enhanced degradation of clay-associated organic carbon has been observed under certain conditions. The conditions in which clay influences microbial decomposition remain uncertain because the mechanisms of clay-organic carbon interactions are not fully understood. Here we reveal the spatiotemporal dynamics of carbon sorption and release within model clay aggregates and the role of enzymatic decomposition by directly imaging a transparent smectite clay on a microfluidic chip. We demonstrate that clay-carbon protection is due to the quasi-irreversible sorption of high molecular-weight sugars within clay aggregates and the exclusion of bacteria from these aggregates. We show that this physically-protected carbon can be enzymatically broken down into fragments that are released into solution. Further, we suggest improvements relevant to soil carbon models.Introduction
Soil constitutes a vast carbon reservoir that exchanges around 60 gigatons of carbon annually with the atmosphere and absorbs about 20% of anthropogenic carbon emissions1,2,3. Consequently, variations in the capacity of soils to store carbon have tremendous impacts on the global carbon cycle and future climate4,5. This sensitivity of global climate to soil carbon storage presents both an obvious risk and a potentially powerful carbon mitigation tool6.The abundance of certain clays and clay minerals (in particular, smectites and nano-crystalline iron and aluminum oxides) is widely recognized as a key factor controlling the amount of carbon stored in soil and its release rate7,8,9, yet the detailed processes responsible for this mineral protection remain unclear, especially in the presence of soil microbes and extracellular enzymes that degrade organic matter1,5,10. One of the common hypotheses is that sorption of organic molecules to clay surfaces temporarily protects this carbon from microbial decomposition11,12,13.
Consequently, recently developed global and field-scale soil carbon models include a protected carbon pool determined by clay abundance and represented as a reversible sorption process5,14. This conceptual view, however, is challenged by evidence showing that clay-associated carbon remains remarkably labile and can be released in a short period of time (days), likely due to microbial and enzymatic activity, if low molecular-weight sugars (e.g. within root exudates) are input into the soil15,16,17. This phenomenon, hereinafter referred to as priming, suggests that microbial and extracellular enzymatic activity may directly impact the efficacy of mineral protection, in contrast with extant soil carbon models that represent mineral protection and biotic processes as independent and uncorrelated phenomena5,18.
Direct observations of the interactions between clay, carbon, microorganisms, and extracellular enzymes (exoenzymes) are needed to improve global soil carbon and climate predictions and to enable effective designs of soil-based climate mitigation strategies10,15,16,17. Such observations are scarce due to a lack of real-time technology to visualize carbon dynamics within clay micro-aggregates, where most organic matter is stored15,19,20. Because of the opaque nature of clay micro-aggregates, observations of organic carbon within these aggregates have typically relied on destructive techniques that provide only a static snapshot of carbon–clay associations, i.e., a 2D or 3D image at a single point of time21,22,23. While these static snapshots provide useful information regarding the pore structure and the carbon distribution within clay aggregates, they provide only indirect insight into the dynamics of clay–carbon protection and release processes represented by soil carbon models10.
Here, we demonstrate how carbon is stored in clay micro-aggregates and later released by exoenzymes in a model soil-on-a-chip24: a microfluidic device containing water, clay, and organic molecules designed to approximate organic sorption in soil. For the first time, we achieved four-dimensional (4D, three spatial dimensions plus time), imaging of carbon and bacteria within and surrounding clay aggregates by combining fluorescently labeled carbon and microbes with a transparent synthetic smectite clay (laponite) and confocal microscopy. With this 4D imaging method, we investigate the sorption of sugars with different molecular weights to smectite clay and show that high molecular-weight sugars (polysaccharides) are quasi-irreversibly sorbed within clay aggregates, i.e., we observe essentially no desorption on the time-scale of our experiments.
In contrast, low molecular-weight sugars such as glucose are reversibly sorbed to clay. We find that this sorption creates a spatial separation, hence likely a physical protection, between the complex organic matter sorbed within clay aggregates and microorganisms confined to the periphery. Finally, we study how exoenzymes can rapidly promote the release of protected carbon. Based on our measurements, we propose an integrated view of how clay, bacteria, and exoenzymes together affect soil carbon storage and release and suggest an improved model structure for soil carbon predictions.
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