Niche adaptation of particle-associated ammonia-oxidizing archaea sustains nitrification under marine deoxygenation

Marine deoxygenation is restructuring coastal microbial niches and metabolic networks, with cascading effects on biogeochemical cycles, a key component of which is the nitrogen cycle. Particles constitute a critical ecological interface that mediates microbial niche partitioning and oxygen-sensitive balance between nitrogen loss and retention in deoxygenating coastal waters. However, the niche-dependent metabolic partitioning of microbial communities and its influence on the nitrogen cycle under deoxygenation remains poorly constrained. We conducted a 22-day field investigation of the deoxygenated water column off the Zhoushan coast, China, combining temporal 15 N-tracer-based nitrification rate measurements with size-fractionated metagenomic sequencing during the day of the most severe bottom-water oxygen depletion. Our data revealed a nitrification hotspot in the low-oxygen waters below the pycnocline, with persistently elevated rates and an enriched abundance of ammonia-oxidizing archaea (AOA) and nitrite-oxidizing bacteria. Notably, particle-associated AOA exhibited significantly enriched genomic potential for coupled nitrogen cycling and carbon fixation, while the dominant groups adapted to low-oxygen particles via distinct metabolic strategies. Nitrosomarinus -like AOA exhibited higher gene counts ( amoA -normalized) for ammonia ( amt ) and high-affinity phosphate ( pst ) transporters, whereas their Water column group A-like counterparts were enriched in low-affinity phosphate transporters ( pit ). Urease gene enrichment in both major AOA clades implicates urea as an ecologically relevant alternative nitrogen source for ammonia acquisition in coastal waters. Furthermore, particle-associated AOA may couple nitrite production and consumption via co-enriched ammonium monooxygenase ( amoA ) and nitrite reductase ( nirK ), potentially increasing nitrogen loss through local nitrite utilization. Collectively, our findings demonstrate that differential adaptation across clades underpins the pivotal role of AOA in nitrogen cycling under deoxygenation.