Taxonomic and carbon metabolic diversification of Bathyarchaeia during its co-evolution history with the early Earth surface environment

Bathyarchaeia, as one of the most abundant microorganisms on Earth, play vital roles in the global carbon cycle. However, our understanding of their origin, evolution and ecological functions remains poorly constrained. Based on the phylogeny of the present largest dataset of Bathyarchaeia metagenome assembled genome (MAG), we reclassified Bathyarchaeia into eight order-level units and corresponded to the former subgroup system. Highly diversified and versatile carbon metabolisms were discovered among different orders, particularly atypical C1 metabolic pathways, indicating that Bathyarchaeia represent overlooked important methylotrophs. Molecular dating results indicate that Bathyarchaeia diverged at ∼3.3 Ga, followed by three major diversifications at ∼3.0 Ga, ∼2.5 Ga and ∼1.8-1.7 Ga, likely driven by continental emergence, growth and intensive submarine volcanism, respectively. The lignin-degrading Bathyarchaeia clade emerged at ∼300 Ma and perhaps contributed to the sharply decreased carbon sequestration rate during the Late Carboniferous period. The evolutionary pathway of Bathyarchaeia potentially have been shaped by geological forces, which in turn impacted the Earth’s surface environment. Teaser The origin and divergence of Bathyarchaeia linked to the early Earth tectonics and surface environment changes