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.

Summary Despite the increasing reports of non‐cyanobacterial diazotrophs (NCDs) in pelagic waters, only one NCD (GammaA) has been relatively well described, whose genome and physiology are still unclear. Here we present a comprehensive analysis of the biogeography and ecophysiology of a widely distributed NCD, Gamma4. Gamma4 was the most abundant Gammaproteobacterial NCD along transects across the subtropical North Pacific. Using quantitative PCR, Gamma4 was detectable throughout the surface waters of North Pacific (7°N–55°N, 138°E–80°W), whereas GammaA was detected at <2/3 of the stations. Gamma4 was abundant during autumn‐winter and positively correlated with chlorophyll a, while GammaA thrived during spring‐summer and was positively correlated with temperature. Environmental clones affiliated with Gamma4 were widely detected in pelagic waters, oxygen minimum zones and even dinoflagellate microbiomes. By analysing the metabolic potential of a genome of Gamma4 reconstructed from the Tara Oceans dataset, we suggest that Gamma4 is a versatile heterotrophic NCD equipped with multiple strategies in scavenging phosphate (and iron) and for respiratory protection of nitrogenase. The transcription of nitrogenase genes is putatively regulated by Fnr‐NifL‐NifA and GlnD‐GlnK systems that respond to intracellular oxygen and glutamate concentration. These results provide important implications for the potential life strategies of pelagic NCDs.

Summary 27In the study, we used miTAG approach to analyse the distributional pattern of the ammonium 28 oxidizing archaea (AOA) lineages in the global oceans using the metagenomics datasets of 29 the Tara Oceans global expedition (2009)(2010)(2011)(2012)(2013)