Ammonium loss microbiologically mediated by Fe(III) and Mn(IV) reduction along a coastal lagoon system

Anaerobic ammonium oxidation, associated with both iron (Feammox) and manganese (Mnammox) reduction, is a microbial nitrogen (N) removal mechanism recently identified in natural ecosystems. Nevertheless, the spatial distributions of these non-canonical Anammox (NC-Anammox) pathways and their environmental drivers in subtidal coastal sediments are still unknown. Here, we determined the potential NC-Anammox rates and abundance of dissimilatory metal-reducing bacteria (Acidomicrobiaceae A6 and Geobacteraceae) at different horizons (0-20 cm at 5 cm intervals) of subtidal coastal sediments using the ¹⁵N isotope-tracing technique and molecular analyses. Sediments were collected across three sectors (inlet, transition, and inner) in a coastal lagoon system (Bahia de San Quintin, Mexico) dominated by seagrass meadows. The positive relationship between ³⁰N₂ production rates and dissimilatory Fe and Mn reduction provided evidence for Feammox's and Mnammox's co-occurrence. N loss through NC-Anammox was detected in subtidal sediments, with potential rates of 0.07-0.62 μg N g^-1 day^-1. NC-Anammox process in vegetated sediments tended to be higher than those in adjacent unvegetated ones. NC-Anammox rates showed a subsurface peak (between 5 and 15 cm) in the vegetated sediments but decreased consistently with depth in the adjacent bare bottoms. Thus, the presence/absence of seagrasses and sediment characteristics, particularly the availability of organic carbon and microbiologically reducible Fe(III) and Mn(IV), affected the abundance of dissimilatory metal-reducing bacteria, which mediated NC-Anammox activity and the associated N removal. An annual loss of 32.31 ± 3.57 t N was estimated to be associated with Feammox and Mnammox within the investigated area, accounting for 2.8-4.7% of the gross total import of reactive N from the ocean into the Bahia de San Quintin. Taken as a whole, this study reveals the distribution patterns and controlling factors of the NC-Anammox pathways along a coastal lagoon system. It improves our understanding of the coupling between N and trace metal cycles in coastal environments.