Close spatial and metabolic association between heterotrophic and ammonia-oxidizing marine Nitrososphaerota

Following the ubiquitous autotrophic ammonia-oxidizing archaea (AOA), heterotrophic representatives of the marine Nitrososphaerota (HMN) form the second most abundant group within this archaeal phylum. However, their eco-evolutionary strategies remain poorly understood. Previous studies have reported a consistent co-occurrence of HMN with marine AOA (MAOA), prompting a detailed investigation into their potential interaction. Through large-scale (meta)genomic and metatranscriptomic analyses, we reveal that HMN possess ultra-streamlined genomes and globally co-occur with marine AOA. The absence of most B vitamin biosynthesis pathways, incomplete citrate cycle and glycolysis, along with the essential requirement for exogenous amino acids, suggest their potential metabolic dependency on AOA. Meanwhile, catalyzed reporter deposition fluorescence in situ hybridization supports a close physical association between HMN and AOA. The nearly synchronous origins of HMN and AOA after oxygen rise, coupled with HMN's dispersive microhabitats (evidenced by dense, shallow subclades) and extensive horizontal gene transfer between these groups, further support their close relationship-although HMN likely acquired heterotrophic capabilities from bacteria. This study reveals a previously unrecognized association between HMN and AOA, implying a tight coupling between autotrophic and heterotrophic processes in deep-sea habitats.