Millimeter-scale niche differentiation of N-cycling microorganisms across the soil-water interface has implications for N2O emissions from wetlands

Wetlands can be a significant source of N2O under current global climate change regime with the soil-water interface representing a biogeochemical hotspot for microbial activity. However, the role of soil-water interface in controlling N2O emissions remains poorly understood. We hypothesized that the millimeter-scale redox gradient across the soil-water interface generates corresponding distinct niche for N-cycling microorganisms that collectively regulate the production and consumption of N2O over the same spatial scale. The abundance, transcriptional activity and spatial organization of different N-cycling guilds across the soil-water interface were characterized in mesocosms from three different paddy soils with different N2O emissions. Results demonstrated millimeter-scale stratification of N-cycling microbial activity across the soil-water interface, and in particular within the first 10 mm of flooded soils. Ammonia-oxidizing microorganisms were only transcriptionally active in the top 4 mm, suggesting a previously underestimated contribution to N2O emissions from wetlands. Variation in N2O accumulation was observed across the soil-water interface, with the highest concentrations measured at either the soil-water interface or in the deeper anoxic layer of paddy soils. Despite this difference, N2O-reducing microorganisms exhibited high transcriptional activity at the soil-water interface in all soils, suggesting that there is a microbial-mediated sink for N2O across the soil-water interface that can reduce N2O produced from both oxic and anoxic layers. This work demonstrate an underappreciated and essential role of the microbial hot zones at soil-water interface in regulating N2O emissions from wetlands.