Genomic determinants of soil depth niche partitioning in Gagatemarchaeaceae, a novel family of deeply-rooted Thaumarchaeota

Knowledge of deeply-rooted non-ammonia oxidising Thaumarchaeota lineages from terrestrial environments is scarce, despite their abundance in acidic soils. Here, 15 new deeply-rooted thaumarchaeotal genomes were assembled from acidic topsoils (0-15cm) and subsoils (30-60 cm), most of them corresponding to two genera of terrestrially prevalent Gagatemarchaeaceae (previously known as thaumarchaeotal Group I.1c). Unlike previous predictions, metabolic annotations suggest Gagatemarchaeaceae perform aerobic respiration and use various organic carbon sources. Evolutionary speciation between topsoil and subsoil lineages happened early in Gagatemarchaeaceae history, with significant metabolic and genomic trait differences. Reconstruction of the evolutionary mechanisms showed that the genome expansion in topsoil Gagatemarchaeaceae resulted from extensive early lateral gene acquisition, followed by progressive gene duplication throughout evolutionary history. Ancestral trait reconstruction using the expanded genomic diversity also refuted the previous hypothesis of a Thaumarchaeota thermophilic ancestor. Ultimately, this study provides an attractive model for studying mechanisms driving niche partitioning between spatially related ecosystems.