Microbial communities overwhelm environmental controls in explaining nitrous oxide emission in acidic soils

Abstract

Intensively fertilized acidic soils are global hotspots of nitrous oxide (N2O) emissions, contributing to net agronomic greenhouse gas outcomes. Identifying the key drivers of soil N2O emissions is hampered by the synergistic or antagonistic effects of multiple factors. Within a framework based on the predominant role of microbial communities producing N2O, the N2O emissions are affected either by proximal regulators: temporary soil property fluctuations affect N2O production transcriptionally, or by distal regulators: persistent genetic rearrangements in local microbial communities. The proximal regulators, individually or together, may spontaneously impact distal regulators. Here, we use acidic soils from tea (Camellia sinensis L.) plantations on a broader geographic scale as a model system. Based on amplicon sequencing and properties of 195 acidic (average pH = 5.0) soils, we determined the importance of proximal and distal regulation to N2O emissions. Microbial phylogenetic diversity as a distal regulator overwhelms mineral N content as a proximal regulator in explaining high N2O emissions. Low-abundance, diverse prokaryotic communities (e.g., Acidothermu) and specialized denitrifying fungal communities (e.g., Fusarium) were associated with high N2O emissions. Revisiting the impact of proximal regulators on distal regulators revealed that soil pH is the sole proximal regulator influencing the prokaryotic rare taxa that correlated with high N2O emissions. When considering proximal regulators together (here soil properties compiled as soil fertility index), the microbial diversity were independent of soil fertility. The microbial assembly was dominated by stochastic processes. Consequently, proximal regulators have a limited impact on distal regulators of N2O emissions from acidic soils. In conclusion, the framework underscored the importance of in situ microbial communities as distal regulators in explaining high N2O emissions from acidic soils.