Genomic Characteristics of a Novel Species of Ammonia-Oxidizing Archaea from the Jiulong River Estuary

Ammonia-oxidizing archaea (AOA) are ubiquitous in diverse ecosystems and play a pivotal role in global nitrogen and carbon cycling. Although AOA diversity and distribution are widely studied, mainly based on the amoA (alpha subunit of ammonia monooxygenase) genotypes, only limited investigations have addressed the relationship between AOA genetic adaptation, metabolic features, and ecological niches, especially in estuaries. Here, we describe the AOA communities along the Jiulong River estuary in southern China. Nine high-quality AOA metagenome-assembled genomes (MAGs) were obtained by metagenomics. Five of the MAGs are proposed to constitute a new species, "Candidatus Nitrosopumilus aestuariumsis" sp. nov., based on the phylogenies of the 16S and 23S rRNA genes and concatenated ribosomal proteins, as well as the average amino acid identity. Comparative genomic analysis revealed unique features of the new species, including a high number of genes related to diverse carbohydrate-active enzymes, phosphatases, heavy-metal transport systems, flagellation, and chemotaxis. These genes may be crucial for AOA adaptation to the eutrophic and heavy-metal-contaminated Jiulong River estuary. The uncovered detailed genomic characteristics of the new estuarine AOA species highlight AOA contributions to ammonia oxidation in the Jiulong River estuary. IMPORTANCE In this study, AOA communities along a river in southern China were characterized, and metagenome-assembled genomes (MAGs) of a novel AOA Glade were also obtained. Based on the characterization of AOA genomes, the study suggests adaptation of the novel AOAs to estuarine environments, providing new information on the ecology of estuarine AOA and the nitrogen cycle in contaminated estuarine environments.