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

Abstract

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.

Widespread Bathyarchaeia encode a novel methyltransferase utilizing lignin‐derived aromatics

“…B. ligniniphilus was mesophilic, with an optimum growth temperature of 20°C (Figure S1); their cells appeared as small cocci with a diameter of ~500 nm and occurred individually or in chain‐like aggregates of several cells (Figure S2). Members of Bathyarchaeia were previously classified into 25 subgroups 17 , which are now assigned into eight orders 22,23 . Phylogenetic inferences placed Ca .…”

“…More than half (172/297) of the bathyarchaeial MAGs belonged to the order Baizomonadales, which are phylogenetically diverse (Figure 2 and Table S5) 20,22,23 . Additionally, more than a third of the MAGs (60/172) in the order Baizomonadales contained the mtgB gene or its gene cluster; these MAGs were assembled from diverse anoxic habitats, including termite guts, mangrove sediments, subsurface fracture fluids, permafrost active layer soils, marine sediments, peatlands, peat soils, estuary sediments, hot spring sediments, and mud volcanos.…”

“…In 297 bathyarchaeial MAGs, 60 MAGs were found to contain the Bathyarchaeia-specific mtgB gene or its gene cluster; intriguingly, all 60 MAGs clustered in the order Baizomonadales 22,23 (Figure 2 and Table S5). Thus, the evolution model of Bathyarchaeia-specific mtgB genes may be vertical inheritance because they likely evolved from the common ancestor of the order Baizomonadales.…”

“…Ca. B. ligniniphilus belongs to the formerly assigned subgroup Bathy-8 and is currently assigned to the family Baizostellaceae in the order Baizomonadales 20,23 . Bathy-8 (or family Baizostellaceae) is frequently detected in high abundances in coastal sediments, especially in deep sediment layers with low redox potential, and lacks electron acceptors 16,19,[26][27][28] .…”

Why and how to use the SeqCode

“…However, the Archaea remain largely mysterious as the majority are uncultivated and have no cultured close relatives. Thus, MAGs and SAGs provide access to their genomes and enable inferring key genes for specific functions, metabolism, and phylogenetic relationships [40][41][42] . Analyses of MAGs have provided strong evidence that members of the Asgard lineage of Archaea may be the closest prokaryotic ancestor to the "nuclear" component of the Eukarya 43,44 .…”