Anaerobic Ammonium Oxidation Linked to Microbial Reduction of Natural Organic Matter in Marine Sediments

Identification of microbial processes driving the loss of nitrogen from the oceans is of paramount relevance as these processes affect primary productivity in these ecosystems, which ultimately affects global biogeochemical cycles. Denitrification and anammox (anaerobic ammonium oxidation coupled to nitrite reduction) are the only identified processes so far that lead to nitrogen loss in marine environments. Here we provide stoichiometric and spectroscopic evidence, as well as tracer analysis with [15N]­ammonium, revealing that anaerobic ammonium oxidation linked to the microbial reduction of natural organic matter (NOM) fuels nitrogen loss in marine sediments from the eastern tropical North Pacific coast. Tracer analysis revealed that the NOM-dependent anammox process was responsible for producing ∼1.5 μg of 15N2 (g of sediment)−1 day–1 after incubation for 27 days in sediment incubations amended with Pahokee peat, while intrinsic NOM present in the sediment promoted the production of ∼0.4 μg of 15N2 (g of sediment)−1 day–1. Taxonomic characterization, based on 16S rRNA gene sequencing, of the biota present in marine sediments performing the NOM-dependent anammox process revealed several microbial members are potentially involved. The most predominant bacterial phylotypes detected were associated with Phycisphaeraceae, Actinomarinales, Acidiferrobacteraceae, and Rhodobacteraceae, while Nitrosopumilaceae was the only archaeal family whose level clearly increased during the course of NOM-dependent anammox. This is a novel pathway interconnecting the oceanic biogeochemical cycles of N and C, which may significantly propel nitrogen fluxes in organic-rich, coastal marine sediments