Visualization and quantification of carbon "rusty sink" by rice root iron plaque: Mechanisms, functions, and global implications

Abstract

Paddies contain 78% higher organic carbon (C) stocks than adjacent upland soils, and iron (Fe) plaque formation on rice roots is one of the mechanisms that traps C. The process sequence, extent and global relevance of this C stabilization mechanism under oxic/anoxic conditions remains unclear. We quantified and localized the contribution of Fe plaque to organic matter stabilization in a microoxic area (rice rhizosphere) and evaluated roles of this C trap for global C sequestration in paddy soils. Visualization and localization of pH by imaging with planar optodes, enzyme activities by zymography, and root exudation by ¹⁴ C imaging, as well as upscale modeling enabled linkage of three groups of rhizosphere processes that are responsible for C stabilization from the micro- (root) to the macro- (ecosystem) levels. The ¹⁴ C activity in soil (reflecting stabilization of rhizodeposits) with Fe²⁺ addition was 1.4-1.5 times higher than that in the control and phosphate addition soils. Perfect co-localization of the hotspots of β-glucosidase activity (by zymography) with root exudation (¹⁴ C) showed that labile C and high enzyme activities were localized within Fe plaques. Fe²⁺ addition to soil and its microbial oxidation to Fe³⁺ by radial oxygen release from rice roots increased Fe plaque (Fe³⁺ ) formation by 1.7-2.5 times. The C amounts trapped by Fe plaque increased by 1.1 times after Fe²⁺ addition. Therefore, Fe plaque formed from amorphous and complex Fe (oxyhydr)oxides on the root surface act as a "rusty sink" for organic matter. Considering the area of coverage of paddy soils globally, upscaling by model revealed the radial oxygen loss from roots and bacterial Fe oxidation may trap up to 130 Mg C in Fe plaques per rice season. This represents an important annual surplus of new and stable C to the existing C pool under long-term rice cropping.

Keywords: Fe-oxidizing and Fe-reducing bacteria; carbon sequestration; enzyme activity; fluctuating redox conditions; iron plaque; rhizosphere processes.