Availability of fixed nitrogen is a pivotal driver on primary productivity in the oceans, thus the identification of key processes triggering nitrogen losses from these ecosystems is of major importance as they affect ecosystems function and consequently global biogeochemical cycles. Denitrification and anaerobic ammonium oxidation coupled to nitrite reduction (Anammox) are the only identified marine sinks for fixed nitrogen. The present study provides evidence indicating that anaerobic ammonium oxidation coupled to the reduction of sulfate, the most abundant electron acceptor present in the oceans, prevails in marine sediments. Tracer analysis with N-ammonium revealed that this microbial process, here introduced as Sulfammox, accounts for up to 5 μgN produced g day in sediments collected from the eastern tropical North Pacific coast. Raman and X-ray diffraction spectroscopies revealed that elemental sulfur and sphalerite (ZnFeS) were produced, besides free sulfide, during the course of Sulfammox. Anaerobic ammonium oxidation linked to Fe(III) reduction (Feammox) was also observed in the same marine sediments accounting for up to 2 μg N produced g day. Taxonomic characterization, based on 16S rRNA gene sequencing, of marine sediments performing the Sulfammox and Feammox processes revealed the microbial members potentially involved. These novel nitrogen sinks may significantly fuel nitrogen loss in marine environments. These findings suggest that the interconnections among the oceanic biogeochemical cycles of N, S and Fe are much more complex than previously considered.

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.

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In the present study, the capacity of enrichments derived from marine sediments collected from different sites of the Mexican littoral to perform anaerobic ammonium oxidation (anammox) coupled to sulfide-dependent denitrification for simultaneous removal of ammonium and sulfide linked to nitrite reduction was evaluated. Sulfide-dependent denitrification out-competed anammox during the simultaneous oxidation of sulfide and ammonium. Significant accumulation of elemental sulfur (ca. 14-30 % of added sulfide) occurred during the coupling between the two respiratory processes, while ammonium was partly oxidized (31-47 %) due to nitrite limitation imposed in sediment incubations. Nevertheless, mass balances revealed up to 38 % more oxidation of the electron donors available (ammonium and sulfide) than that expected from stoichiometry. Recycling of nitrite, from nitrate produced through anammox, is proposed to contribute to extra oxidation of sulfide, while additional ammonium oxidation is suggested by sulfate-reducing anammox (SR-anammox). The complex interaction between nitrogenous and sulfurous compounds occurring through the concomitant presence of autotrophic denitrification, conventional anammox and SR-anammox may significantly drive the nitrogen and sulfur fluxes in marine environments.

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