Langwig, Marguerite

Abstract Asgard archaea were pivotal in the origin of complex cellular life. Hodarchaeales (Asgardarchaeota class Heimdallarchaeia) were recently shown to be the closest relatives of eukaryotes. However, limited sampling of these archaea constrains our understanding of their ecology and evolution 1–3 , including their anticipated role in eukaryogenesis. Here, we nearly double the number of Asgardarchaeota metagenome-assembled genomes (MAGs) to 869, including 136 new Heimdallarchaeia (49 Hodarchaeales) and several novel lineages. Examining global distribution revealed Hodarcheales are primarily found in coastal marine sediments. Detailed analysis of their metabolic capabilities revealed guilds of Heimdallarchaeia are distinct from other Asgardarchaeota. These archaea encode hallmarks of aerobic eukaryotes, including electron transport chain complexes (III and IV), biosynthesis of heme, and response to reactive oxygen species (ROS). The predicted structural architecture of Heimdallarchaeia membrane-bound hydrogenases includes additional Complex-I-like subunits potentially increasing the proton motive force and ATP synthesis. Heimdallarchaeia genomes encode CoxD, which regulates the electron transport chain (ETC) in eukaryotes. Thus, key hallmarks for aerobic respiration may have been present in the Asgard-eukaryotic ancestor. Moreover, we found that Heimdallarchaeia is present in a variety of oxic marine environments. This expanded diversity reveals these Archaea likely conferred energetic advantages during early stages of eukaryogenesis, fueling cellular complexity.

Abstract Microbes are the most abundant form of life on Earth and play crucial roles in carbon and nutrient cycling. Despite their crucial role, our understanding of microbial diversity and physiology on the ocean floor is limited. To address this gap in knowledge, we obtained 55 novel bacterial metagenome-assembled genomes (MAGs) from coastal and deep sea sediments. Phylogenomic analyses revealed they belong to four new and one poorly described bacterial phyla. Comparison of their rRNA genes with public databases revealed they are all globally distributed. These novel bacteria are capable of the anaerobic degradation of polysaccharides and proteins, and the respiration of sulfur and nitrogen. These genomes code for an unusually high proportion (~ 9, and up to 20% per genome) of protein families lacking representatives in public databases. Hundreds of these protein families are predicted to be co-localized with genes for sulfur reduction, nitrogen cycling, energy conservation, and the degradation of organic compounds. These findings expand our understanding of microbial diversity and link previously overlooked gene families with key metabolic processes in the oceans.