Discovery of Candidatus Nitrosomaritimum as a New Genus of Ammonia-Oxidizing Archaea Widespread in Anoxic Saltmarsh Intertidal Aquifers

Ammonia-oxidizing archaea (AOA) are widely distributed in marine and terrestrial habitats, contributing significantly to global nitrogen and carbon cycles. However, their genomic diversity, ecological niches, and metabolic potentials in the anoxic intertidal aquifers remain poorly understood. Here, we discovered and named a novel AOA genus, Candidatus Nitrosomaritimum, from the intertidal aquifers of Yancheng Wetland, showing close metagenomic abundance to the previously acknowledged dominant Nitrosopumilus AOA. Further construction of ammonia monooxygenase-based phylogeny demonstrated the widespread distribution of Nitrosomaritimum AOA in global estuarine-coastal niches and marine sediment. Niche differentiation among sublineages of this new genus in anoxic intertidal aquifers is driven by salinity and dissolved oxygen gradients. Comparative genomics revealed that Candidatus Nitrosomaritimum has the genetic capacity to utilize urea and possesses high-affinity phosphate transporter systems (phnCDE) for surviving phosphorus-limited conditions. Additionally, it contains putative nosZ genes encoding nitrous-oxide (N2O) reductase for reducing N2O to nitrogen gas. Furthermore, we gained first genomic insights into the archaeal phylum Hydrothermarchaeota populations residing in intertidal aquifers and revealed their potential hydroxylamine-detoxification mutualism with AOA through utilizing the AOA-released extracellular hydroxylamine using hydroxylamine oxidoreductase. Together, this study unravels the overlooked role of priorly unknown but abundant AOA lineages of the newly discovered genus Candidatus Nitrosomaritimum in biological nitrogen transformation and their potential for nitrogen pollution mitigation in coastal environments.