Ammonia-oxidizing archaea (AOA) are key for the transformation of ammonia to oxidized forms of nitrogen in aquatic environments around the globe, including nutrient-rich coastal and estuarine waters such as San Francisco Bay (SFB). Using metagenomics and 16S rRNA gene amplicon libraries, we found that AOA are more abundant than ammonia-oxidizing bacteria (AOB) and nitrite-oxidizing bacteria (NOB), except in the freshwater stations in SFB. In South SFB, we observed recurrent AOA blooms of "Candidatus Nitrosomarinus catalina" SPOT01-like organisms, which account for over 20% of 16S rRNA gene amplicons in both surface and bottom waters and co-occur with weeks of high nitrite concentrations (>10 μM) in the oxic water column. We observed pronounced nitrite peaks occurring in the autumn for 7 of the last 9 years (2012 to 2020), suggesting that seasonal AOA blooms are common in South SFB. We recovered two high-quality AOA metagenome-assembled genomes (MAGs), including a Nitrosomarinus-like genome from the South SFB bloom and another Nitrosopumilus genome originating from Suisun Bay in North SFB. Both MAGs cluster with genomes from other estuarine/coastal sites. Analysis of Nitrosomarinus-like genomes show that they are streamlined, with low GC content and high coding density, and harbor urease genes. Our findings support the unique niche of Nitrosomarinus-like organisms which dominate coastal/estuarine waters and provide insights into recurring AOA blooms in SFB. IMPORTANCE Ammonia-oxidizing archaea (AOA) carry out key transformations of ammonia in estuarine systems such as San Francisco Bay (SFB)-the largest estuary on the west coast of North America-and play a significant role in both local and global nitrogen cycling. Using metagenomics and 16S rRNA gene amplicon libraries, we document a massive, recurrent AOA bloom in South SFB that co-occurs with months of high nitrite concentrations in the oxic water column. Our study is the first to generate metagenome-assembled genomes (MAGs) from SFB, and through this process we recovered two high-quality AOA MAGs, one of which originated from bloom samples. These AOA MAGs yield new insight into the Nitrosopumilus and Nitrosomarinus-like lineages and their potential niches in coastal and estuarine systems. Nitrosomarinus-like AOA are abundant in coastal regions around the globe, and we highlight the common occurrence of urease genes, low GC content, and range of salinity tolerances within this lineage.
Keywords: Thaumarchaeota; ammonia-oxidizing archaea; bloom; estuary; metagenome-assembled genome; nitrification; pelagic.