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

TL;DR

This study shows how ammonia-oxidizing archaea adapt to low-oxygen marine environments, supporting nitrification and influencing nitrogen cycling in coastal waters.

Contribution

The study reveals niche-specific metabolic adaptations of particle-associated ammonia-oxidizing archaea under marine deoxygenation.

Findings

Nitrification hotspots were observed in low-oxygen waters with enriched ammonia-oxidizing archaea and nitrite-oxidizing bacteria.

Particle-associated AOA showed distinct genomic traits for nitrogen cycling and carbon fixation compared to water column AOA.

Urease gene enrichment suggests urea is a key nitrogen source for AOA in deoxygenated coastal waters.

Abstract

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 15N-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.

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