Anammox bacteria drive fixed nitrogen loss in hadal trench sediments

Abstract

Benthic N2 production by microbial denitrification and anammox is the largest sink for fixed nitrogen in the oceans. Most N2 production occurs on the continental shelves, where a high flux of reactive organic matter fuels the depletion of nitrate close to the sediment surface. By contrast, N2 production rates in abyssal sediments are low due to low inputs of reactive organics, and nitrogen transformations are dominated by aerobic nitrification and the release of nitrate to the bottom water. Here, we demonstrate that this trend is reversed in the deepest parts of the oceans, the hadal trenches, where focusing of reactive organic matter enhances benthic microbial activity. Thus, at ∼8-km depth in the Atacama Trench, underlying productive surface waters, nitrate is depleted within a few centimeters of the sediment surface, N2 production rates reach those reported from some continental margin sites, and fixed nitrogen loss is mainly conveyed by anammox bacteria. These bacteria are closely related to those known from shallow oxygen minimum zone waters, and comparison of activities measured in the laboratory and in situ suggest they are piezotolerant. Even the Kermadec Trench, underlying oligotrophic surface waters, exhibits substantial fixed N removal. Our results underline the role of hadal sediments as hot spots of deep-sea biological activity, revealing a fully functional benthic nitrogen cycle at high hydrostatic pressure and pointing to hadal sediments as a previously unexplored niche for anaerobic microbial ecology and diagenesis.

Nitrite accumulation and the associated anammox bacteria niche partitioning in marine sediments

“…1C; See the detailed nitrite and nitrate profiles in individual cores in Supplementary Figure S3). Such accumulation was mainly detected in sediments on the continental slopes [ [27][28][29][30]], along the mid-ocean ridges [31] of the Pacific and Atlantic Oceans, and within hadal trenches in the Pacific [14,32,33] (Fig. 1B).…”

“…1B). Notably, most of these sites also feature a nitrate-ammonium transition zone (NATZ), where the anammox reaction occurs [14,18], suggesting a potential link between anammox bacteria and the observed nitrite accumulation. The nitrite accumulation was likely not detected in the upper few meters of sediments of (i) continental margins because nitrate penetration is too shallow to be properly resolved without dedicated microscale measurements, or (ii) abyssal plains because high concentrations of nitrate and O 2 are present in the porewater throughout the entire sediment columns [e.g., [33][34][35][36]].…”

“…Since its discovery in the marine environment two decades ago [13], anammox has been shown to dominate fixed nitrogen loss [e.g., [14][15][16]] and therefore control global ocean productivity [17]. Among the previously recognized marine anammox bacteria (affiliated with the families Candidatus Brocadiaceae and Candidatus Scalinduaceae), members of Scalinduaceae have been consistently detected in marine sediments [14,16,[18][19][20], with several enrichment cultures obtained from coastal sediments [e.g., Ca. Scalindua japonica [21] and Ca.…”

High Carbon Mineralization Rates in Subseafloor Hadal Sediments—Result of Frequent Mass Wasting

“…Without any biogeochemical interpretation, both partial sulfate profiles were used to document a recent mass displacement event only. Furthermore, only three studies exist to date with data from deep-sea trenches that contain pore water information from a maximum depth of 30 cm below the seafloor (Glud et al, 2013(Glud et al, , 2021Hu et al, 2021;Thamdrup et al, 2021).…”

Benthic nitrogen cycling in the deep ocean of the Kuroshio Extension region

“…Compared with coastal or continental shelf sediment, although the total nitrogen loss rate is relatively low, the psychrophilic and autotrophic anammox processes seem to show a rather substantial contribution to N-loss with increasing water depth (Dalsgaard et al, 2005;Devol, 2015). Thamdrup et al (2021) first investigated the benthic N-loss in two hadal trenches, Atacama and Kermadec, with water depths of 7,720-7,915 and 9,300-9,555 m, respectively, which is currently the N-loss result with the greatest water depth reported in the marine sediment. Despite being the deepest part of the ocean, hadal trenches receive both vertical and lateral inputs of organic matter and are believed to be the hotspots for benthic early diagenesis and N-loss processes in deep marine environments (Glud et al, 2021;Thamdrup et al, 2021).…”