Benthic nitrogen cycling in hadal trenches: High rates and large contributions from anammox

Due to low input of reactive organics and resulting deep oxygen penetration, nitrogen cycling in abyssal sediments is generally dominated by aerobic nitrification and the benthic release of nitrate, while relatively little bioavailable N is converted to N₂ by anaerobic denitrification and anammox. By contrast, hadal sediments may represent hot spots of organic deposition and hence favor anaerobic processes to a larger extent, but little is known about the pathways of N cycling there. We investigated benthic nitrogen cycling along the axis of the Kermadec and Atacama trenches based on geochemical and biomolecular analyses as well as experimental ¹⁵N-based rate measurements. Pore water extraction and microsensor profiling both revealed steep decreases in NO₃^- concentrations below the depth of O₂ penetration, with depletion of NO₃^- already at 5 – 10 cm depth in the Atacama Trench compared to ≥ 15 cm in the Kermadec Trench. As NO₂^- concentrations remained low and NH₄⁺ only accumulated below the NO₃^- zone, these profiles indicate active N₂ production and anaerobic ammonium oxidation. Shipboard incubations with ¹⁵NO₃^-, ¹⁵NO₂^- or ¹⁵NH₄⁺ confirmed denitrification and anaerobic NH₄⁺ oxidation activity with highest potential rates in the nitrogenous zone. Isotope pairing in N₂ further implied that NH₄⁺ was oxidized through the anammox process, which was substantiated by a close correlation between rates and copy numbers of the anammox specific hydrazine synthase (hzs) gene. At most sites, anammox dominated N₂ production with contributions reaching ≥70%. Based on hzs gene sequences, hadal anammox bacteria are closely related to ‘Ca. Scalindua’ from shallower marine habitats. Judged from their activity during the incubations at surface pressure, these bacteria were not heavily impaired by decompression. This was substantiated by in situ incubations with ¹⁵N tracers in the seafloor by means of a benthic lander, which generated patterns and rates of N₂ production consistent with those obtained in the laboratory. We conclude that denitrification and anammox are substantial sinks for fixed nitrogen in hadal sediments with most of the loss conveyed by anammox bacteria that appear to be piezotolerant. Our results demonstrate that high rates of biogeochemical activity persist beyond the oxic surface layer of these systems.