Asgard Archaea and Earth's Oxygenation: Uncovering Key Aspects of Eukaryogenesis

forthcoming

Many aspects of life's evolutionary history remain poorly understood, such as the emergence of complex eukaryotic life. The recent discovery of Asgard archaea in anoxic sediments has provided fundamental insights into this process due to their phylogenetic proximity to eukaryotes and their eukaryote-like protein repertoire. The cultivation of the first two anaerobic organisms from this group, both belonging to the Lokiarchaeia, provided support for their role in eukaryogenesis, especially with the detection of a eukaryote-like actin cytoskeleton. Despite these advances, there are still many unanswered questions, such as what was the environmental context of this process, especially considering that the Great Oxidation Event (GOE) preceded it. Some hypotheses suggest that mitochondria evolved in anoxic conditions, while others propose a link between higher cell complexity and rising oxygen levels. The Asgard archaea now considered closest to eukaryotes, namely the Heimdallarchaeia class and its subgroups Hodarchaeales and Kariarchaeaceae, are the only ones thought to be facultative aerobes, fueling this debate, though no cultured representatives exist. This proposal aims to deepen our understanding of oxygen-related processes in Asgard archaea, focusing on reactive oxygen species, and to use these organisms to better understand the ecological context of the rise of eukaryotic life. This will involve i) cultivation of the first facultative aerobic Asgard archaea, thought to be the closest to eukaryotes, ii) comparative phylogenetic analysis of Asgard archaea proteins involved in coping with oxygen, iii) biochemical characterization of these proteins using heterologous expression, iv) expression of these proteins in genetically tractable anaerobic archaea. This project will provide unique insights into the ecology and cell biology of our archaeal ancestors, leading to a transformative understanding of the environmental and evolutionary context of eukaryogenesis.