Sulfur-Driven Iron Reduction Coupled to Anaerobic Ammonium Oxidation

A new biogeochemical pathway has been suggested to be present in terrestrial ecosystems, linking the nitrogen and iron cycles via ferric iron reduction coupled to anaerobic ammonium oxidation. However, the underlying microbiological process has not been demonstrated to date. Here we report a stable consortium, HJ-4, composed of Anaerospora hongkongensis (85%) and facultative anaerobe, Comamonadaceae (15%), which can process ferrihydrite reduction coupled to anaerobic ammonium oxidation driven by sulfur redox cycling. In this process, A. hongkongensis reduces elemental sulfur, sulfite, and polysulfides to sulfide, which fuels ferrihydrite reduction. Sulfide, elemental sulfur, sulfite, and polysulfides serve as electron shuttles, completing the sulfur cycle between A. hongkongensis and ferrihydrite. In addition, Comamonadaceae shows ammonium oxidation potential under aerobic conditions, with nitrite as the main product. We inferred that Comamonadaceae mediates simultaneous nitrification-denitrification coupled to iron redox cycling through nitrate/nitrite-dependent ferrous oxidation under anaerobic conditions. Hence, we discovered a novel pathway for ferric iron reduction coupled to ammonium oxidation, highlighting the key role of electron shuttles and nitrate/nitrite-dependent ferrous oxidation in this process. The biogeochemical cycling of sulfur, iron, and nitrogen could be coupled in aquatic and terrestrial ecosystems.