Niche partitioning associated intraspecific variation of Thaumarchaeota in the deepest ocean sediments

Deep-sea sediments host abundant Thaumarchaeota that are phylogenetically distinct from their pelagic relatives. However, their ecology and evolutionary adaptations remain largely unknown. Here, we performed metagenomic analyses on samples from different depths of a 750-cm sediment core collected from the Mariana Trench Challenger Deep. The abundance of Thaumarchaeota and archaeal amoA generally decreased with depth, except for an unexpected peak midway through the core. The retrieved thaumarchaeotal metagenome-assembled genomes were classified into diverse phylogenetic clusters affiliated with amoA-NP-γ, amoA-NP-θ and amoA-NP-δ of ammonia-oxidizing Thaumarchaeota and non-ammonia-oxidizing lineages. The most abundant group was nested within amoA-NP-γ, typically prevalent in coastal and shallow habitats, providing clues for niche expansion from marine shallow to hadal environments. This benthic group exhibited within-species genomic variations from the previously proposed Hadal water group, suggesting microdiversification of hadal Thaumarchaeota along with niche separation between benthic and pelagic environments. Evolutionary adaptations accompanying the benthic-to-pelagic transition included reduced genome size, loss of motility/cell adhesion, altered energy metabolism, and different substrate (e.g., ammonium) acquisition and regulation mechanisms. These findings provide novel insights on the evolution of hadal Thaumarchaeota and revealed, for the first time, intraspecies-level genomic variation in Thaumarchaeota linked to the benthic-versus-pelagic niche partitioning in the deep ocean.