Anammox and denitrification separately dominate microbial N-loss in water saturated and unsaturated soils horizons of riparian zones

Abstract

Fertilized agroecosystems may show considerable leaching of the mobile nitrogen (N) compound NO3−, which pollutes groundwater and causes eutrophication of downstream waterbodies. Riparian buffer zones, positioned between terrestrial and aquatic environments, effectively remove NO3− and serve as a hotspot for N2O emissions. However, microbial processes governing NO3− reduction in riparian zones still remain largely unclear. This study explored the underlying mechanisms of various N-loss processes in riparian soil horizons using isotopic tracing techniques, molecular assays, and high-throughput sequencing. Both anaerobic ammonium oxidation (anammox) and denitrification activity were maximized in the riparian fringe rather than in the central zones. Denitrifying anaerobic methane oxidation (damo) process was not detected. Interestingly, both contrasting microbial habitats were separated by a groundwater table, which forms an important biogeochemical interface. Denitrification dominated cumulative N-losses in the upper unsaturated soil, while anammox dominated the lower oxic saturated soil horizons. Archaeal and bacterial ammonium oxidation that couple dissimilatory nitrate reduction to ammonium (DNRA) with a high cell-specific rate promoted anammox even further in oxic subsurface horizons. High-throughput sequencing and network analysis showed that the anammox rate positively correlated with Candidatus ‘Kuenenia’ (4%), rather than with the dominant Candidatus ‘Brocadia’. The contribution to N-loss via anammox increased significantly with the water level, which was accompanied by a significant reduction of N2O emission (∼39.3 ± 10.6%) since N-loss by anammox does not cause N2O emissions. Hence, water table management in riparian ecotones can be optimized to reduce NO3− pollution by shifting from denitrification to the environmentally friendly anammox pathway to mitigate greenhouse gas emissions.