Root exudation and fine texture interact to form anoxic microsites in rhizosphere soil

Abstract

Anoxic microsites – portions of soil without oxygen in a soil that is otherwise oxic – are important but poorly understood controls on critical biogeochemical processes. Plant roots and, specifically their exudates, are theorized to trigger anoxic microsite formation by stimulating soil microbial activity and subsequent oxygen consumption. However, direct observations of this phenomenon remain limited; even less is known about how root exudates interact with factors regulating oxygen supply, such as soil texture, to regulate rhizosphere oxygen dynamics. Here, we used reverse microdialysis to simulate root exudation in two distinctly textured soils (coarse and fine). We delivered ¹³C-labeled model root exudates to soil mesocosms over three diurnal cycles and observed that model root exudates increase anoxic volume during the day, particularly in fine-textured soil, and coincide with periods of enhanced soil microbial respiration and positive priming, and thus oxygen consumption. Targeted metabolomics and dPCR further showed that exudate addition increased the abundance of fermentation products and genes associated with anaerobic metabolisms in the rhizosphere. Overall, our results suggest that limited oxygen supply, combined with increased oxygen demand from positive priming and spatially concentrated microbial respiration of root exudates, contributed to greater anoxic microsite formation and quickly provoked anaerobic metabolisms in the rhizosphere of finer-textured soils. Given that root-induced anoxic microsites are rarely considered in biogeochemical cycles in otherwise well-aerated soils, our results inspire questions about the degree to which anoxic microsites mediate the plant influence on carbon cycling, nutrient availability, and contaminant fate in the rhizosphere.