1262 / 2024-09-20 20:18:13

Candidatus Nitrosomaritimum, an overlooked genus of ammonia-oxidizing archaea in intertidal aquifers and marine sediments

ammonia-oxidizing archaea,nitrogen cycling,Candidatus Nitrosomaritimum,intertidal aquifers

Ammonia-oxidizing archaea (AOA) of the class Nitrososphaeria are ubiquitous canonical chemolithoautotrophs in marine and terrestrial habitats, playing a major role in the global nitrogen and carbon cycles. Despite their significance, the genomic diversity, ecological niches, and metabolic potentials of AOA in the anoxic intertidal aquifers have remained largely unexplored. In this study, we successfully reconstructed 32 metagenome-assembled genomes (MAGs) of Nitrososphaeria from saltmarsh intertidal aquifers in the Yancheng Coastal Wetland, China, and performed large-scale phylogenomic analysis by including 128 Nitrososphaeria-affiliated genomes from various aquatic and terrestrial habitats. We discovered and named a novel AOA genus, Candidatus Nitrosomaritimum, from the intertidal aquifers, 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 sediments. Metatranscriptomic sequencing and amoA gene amplicon sequencing-based analysis indicated that this novel genus is the second most abundant and activate AOA in intertidal aquifers. The niche differentiation of species-level members affiliated with Ca. Nitrosomaritimum and Nitrosopumilus is co-driven by intertidal salinity and dissolved oxygen gradients. Notably, Nitrosomaritimum exhibits the genetic capacity of using urea as an alternative source of ammonia and possesses a putative nitrous oxide (N₂O) reductase responsible for the reduction of N₂O to nitrogen gas, suggesting a putative similar anoxic ammonia oxidation pathway observed in the marine oxygen minimum zones. Moreover, comparative genomic analysis indicated that intertidal AOA genomes selectively carry Pst transporter (pstABCS) or Phn transporter (phnCDE) for the uptake of phosphate. 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. Additionally, it sheds light on their potential metabolic interactions with surrounding microbial communities and genetic adaption to the anoxic conditions of intertidal aquifers.