Microcompartments in archaeal ancestors of eukaryotes: a bioenergetic engine that could have fuelled eukaryogenesis

Abstract

Eukaryotic intracellular compartmentalization is a key innovation in the evolution of complex cellular life. While microcompartments enable metabolic specialization in many bacteria, to our knowledge, no analogous systems have been identified in Archaea. Here, we report the discovery of archaeal microcompartments (AMCs) in Hodarchaeales, an order within the phylum Promethearchaeati (Asgard archaea) that includes the closest known archaeal relatives of eukaryotes. Phylogenetic and structural analyses indicate that these catabolic AMCs, which are specialized for sugar-phosphate metabolism, were acquired by horizontal gene transfer from deep-rooted bacteria of the phylum Myxococcota. The shell pentamers of AMCs are fused to lysine/arginine-rich intrinsically disordered regions that capture cytosolic DNA, facilitating nutrient scavenging. Reaction-diffusion modelling predicts that enzyme colocalization and substrate channelling within AMCs can increase the NADH flux approximately 100-fold. Thus, the AMCs substantially boost energy production in the cell and might have primed the archaeal host for eukaryogenesis.