Are Oxygen Limitations an Under Recognized Regulator of Organic Matter Turnover in Upland Soils?.

Soil plays a critical role in global carbon (C) cycling, having one of the largest dynamic stocks of C on earth stored as soil organic matter (SOM). An important control on the residence time of soil C, which ranges from days to millennia, is the rate at which SOM is mineralized by microbes. It is well recognized that the SOM mineralization rate is regulated by climatic factors in combination with SOM chemistry, mineral-organic associations, and physical protection. Even in seemingly well-drained upland soil systems, the physical structure can impose constraints on oxygen diffusion. But controls on the formation and persistence of anaerobic microsites and their impact on SOM mineralization rates remain poorly understood.  Furthermore, substantial uncertainty exists regarding the contribution of anaerobic metabolism to overall SOM mineralization in upland soils.  

Here we quantitatively place the importance of metabolic constraints in anaerobic microsites on the rate of SOM mineralization in upland soils.  We addressed this challenge using a multi-scale approach, combining field-scale measurements with micro-scale laboratory experiments. In-situ monitoring of a series of upland soils spanning a drainage gradient showed that texture and C bioavailability, in addition to soil moisture status, dictate temporal and spatial dynamics of anaerobic microsites at the pedon-scale. In complimentary laboratory mesocosms, we observed the formation of anaerobic microsites even at moderate moisture contents (60% water-filled pore space). Pore architecture and SOM availability controlled the spatial extent and distribution of anaerobic microsites, which caused a significant reduction in mineralization rates.  Additional experiments in oxygen diffusion-limited reactors showed that such declines in mineralization rates are not only due to lower aerobic respiration, but also a consequence of slower anaerobic metabolism.  Our results indicate that dissimilatory Fe reduction, the predominant respiratory pathway in anaerobic microsites in our system, was limited by supply of secondary metabolites from aerobic zones.  Consistent with thermodynamic predictions, metabolic constraints on C oxidation resulted in the preferential preservation of bioavailable, reduced SOM components in anaerobic microsites.

These findings highlight that oxygen limitations act as a largely unrecognized and greatly underestimated control on overall rates of C oxidation in upland soils.  By incorporating the constraints imposed on microbial metabolism in anaerobic microsites, terrestrial C cycling models will more accurately depict SOM mineralization and storage within soils.