Ecological partitioning and functional specialization of Thermoproteota across multiple trench sediments

Thermoproteota (formerly referred to as Thaumarchaeota) are phylogenetically divided into ammonia-oxidizing archaea (AOA) affiliated with Nitrososphaeria and basal non-ammonia-oxidizing archaea (non-AOA). While both groups co-existed in the hadal trenches, their differentiations across multiple trenches remain poorly understood. Here, 25 medium- and high-quality metagenome-assembled genomes (MAGs), including 18 AOA and 7 non-AOA representatives, were generated from metagenomics of Diamantina, Kermadec, Mariana-Yap trench sediments. AOA MAGs of Nitrosopumilales encompassing CSP1-1, DRGT01 and Nitrosopumilus exhibited chemoautotrophic potential with broader niche widths and higher diversity across trenches. Potential nitrification rates (PNR) were predominantly associated with AOA activity and exhibited clear depth-/trench-dependent patterns, driven by NH₄⁺ availability. In contrast, the non-AOA lineage diverged approximately earlier (∼2.66 Ga), whereas the divergence between B1T1B5 and JAPUIC01 was estimated at ∼1.91 Ga during the Paleoproterozoic. B1T1B5 harbored auto/mixotrophic traits, whereas JAPUIC01 exhibited a metabolically flexible, heterotrophic strategy potentially suited to anaerobic niches. The pronounced niche partitioning and functional specialization of AOA and non-AOA Thermoproteota across geographically isolated trenches were based on their genomic traits, likely an integrated consequence of microbial ecological adaptation and strong purifying selection of the local environmental condition. The findings provide a unified ecological and evolutionary framework for understanding Thermoproteota diversification in the deep ocean and reveals how functional specialization and genomic adaptive evolution shape nitrogen cycling in Earth's deepest ecosystems.