Overlooked Genetic Diversity of Ammonia Oxidizing Archaea Lineages in the Global Oceans

In this study, we used miTAG approach to analyze the distributional pattern and fine-scale genetic diversity of the ammonia oxidizing archaea (AOA) lineages in the global oceans with the metagenomics data sets of the Tara Oceans global expedition (2009-2013). Using the ammonium monooxygenase alpha subunit gene as a biomarker, the AOA communities in the global oceans were recovered with highly diverse operational taxonomic units that affiliated to previously defined clades, including water column A (WCA), water column B (WCB), and SCM1-like clades. In general, the AOA communities were obviously segregated with depth (except the upwelling regions), and the communities in the euphotic zones were more heterogeneous than in the mesopelagic zones (MPZs). The WCA distributed more evenly and widely in the euphotic zone and MPZs, while WCB and SCM1-like clade mainly distributed in MPZ and high-latitude waters, respectively. At fine-scale genetic diversity, SCM1-like and 2 WCA subclades showed distinctive niche separations of distributional pattern. We further divided the AOA subclades into ecological significant taxonomic units (ESTUs), which were delineated from the distribution pattern of their corresponding subclades. For example, ESTUs of WCA have different correlations with depth, nitrate to silicate ratio, and salinity; SCM1-like A was negatively correlated with irradiation, whereas other SCM1-like ESTUs preferred low-temperature and high-nutrient conditions. Our result showed that the previously defined AOA clades and ecotypes consist of highly diverse sublineages, whose diversity might be overlooked in the past. The distribution patterns of different ESTUs imply their ecophysiological characteristics and potential roles in biogeochemical cycling. Plain Language Summary In the ocean, ammonia oxidizing archaea (AOA) are widely distributed microbes that play important roles in the marine nitrogen cycling and the emission of the highly potent greenhouse gas (N2O). However, the majority of the marine AOA are currently uncultivated; the physiology of marine AOA and the factors that mediate their distribution still remain unclear. In this study, we have analyzed the fine-scale phylogenetic diversity and community structures of the AOA in the global ocean. Based on the results, the genetic diversity of marine AOA might be overlooked in the past since highly diverse groups that showed differential distribution patterns in the previously defined AOA ecotypes are found. Besides, by analyzing the correlations of their distributions with the varied environmental conditions in the global oceans, the diverse AOA groups were delineated with particular physiochemical factors. At a finer resolution than the previously defined ecotypes, our findings provide new insights into the determinants and the ecophysiology of the widely distributed but uncultivated AOA groups.