Exploring Sulfate as an Alternative Electron Acceptor: A Potential Strategy to Mitigate N2O Emissions in Upland Arable Soils

Abstract

Agricultural activities are a significant source of nitrous oxide (N2O), accounting for approximately 60% of global emissions, highlighting the urgent need for innovative strategies to mitigate N2O emissions. Microbes conserve nearly as much energy with nitrate (NO3？) as oxygen (O2) respiration under limited O2 availability. Thus, microorganisms prioritize NO3？, limiting exploration of alternative electron acceptors (EAs) to inhibit N2O emissions through NO3？ respiration in upland arable soils. Current approaches remain insufficient, and the interactions between alternative EA reduction and pathways for N2O emissions remain poorly understood. This study evaluated oxidized iron, manganese, and sulfate as alternative EAs to reduce N2O emissions, along with the effects of zero-valent metals (ZVMs). Metal sulfates (MSs) significantly minimized N2O emissions by inhibiting denitrification rather than altering nitrification in microcosms, as supported by isotope mapping and inorganic nitrogen concentrations. Among others, putative complete denitrifiers, N2O reducers, and sulfate reducers were stimulated, whereas ZVMs stimulated N2O emissions and 16S rRNA gene abundance. Moreover, the abundance of denitrifier-related genes (nirK, nirS, norB, and nosZ) consistently decreased under MS treatments, while dsrA mRNA abundance significantly increased. Sulfate (SO42？) addition reshaped the soil microbial community by enriching sulfur-cycling taxa―including sulfate-reducing and sulfur-oxidizing bacteria―while suppressing nitrifiers such as Nitrospira, potentially disrupting nitrification？denitrification coupling. Ureibacillus thermosphaerius, harboring genes for denitrification and SO42？ reduction, increased under MS treatment. These shifts likely redirected electron flow toward SO42？ respiration, reducing NO3？ utilization and contributing to N2O mitigation. Field-based manipulation experiments over 2？years demonstrated the feasibility of MSs in upland arable soils, reducing yield-scaled N2O emissions by 21.5% without compromising crop yields. A systematic literature review and meta-analysis revealed that SO42？ application mitigated N2O emissions by an average of 9%, with over 70% of observations showing a decreasing trend, underscoring its potential as an effective soil amendment for sustainable agriculture.