Evolution of diverse cell division and vesicle formation systems in Archaea

Key Points Recently, the unexpected discovery was made that the hyperthermophilic crenarchaeote Sulfolobus spp. use a novel cell division system that consists of homologues of eukaryotic endosomal secretion complex required for transport III (ESCRT-III) proteins. Comparative genomic analysis shows that Archaea possess at least three distinct membrane remodelling systems, namely, the FtsZ-based bacterial-type systems present in most Euryarchaeota, the ESCRT-III-based system that is responsible for cell division in the Desulphorococcales and the Sulfolobales, and a putative novel system centred around the archaeal actin-related protein in the Thermoproteales. Many archaeal genomes, in particular those of ' Candidatus Korarchaeum cryptophilum', the Thaumarchaeota and some of the Thermococci, encode assortments of components from different membrane remodelling systems. Evolutionary reconstructions suggest that the last common ancestor of the extant archaea possessed a complex membrane remodelling apparatus, different components of which were lost during subsequent evolution of archaeal lineages. Eukaryotes seem to have inherited the ancestral membrane remodelling systems in their entire complexity. In this Analysis article, Makarova and colleagues provide an overview of the cell division and membrane budding systems of the Archaea. They show that at least four different systems regulate these processes, providing insight into the evolutionary history of archaeal and eukaryotic cells. Recently a novel cell division system comprised of homologues of eukaryotic ESCRT-III (endosomal sorting complex required for transport III) proteins was discovered in the hyperthermophilic crenarchaeote Sulfolobus acidocaldarius . On the basis of this discovery, we undertook a comparative genomic analysis of the machineries for cell division and vesicle formation in Archaea. Archaea possess at least three distinct membrane remodelling systems: the FtsZ-based bacterial-type system, the ESCRT-III-based eukaryote-like system and a putative novel system that uses an archaeal actin-related protein. Many archaeal genomes encode assortments of components from different systems. Evolutionary reconstruction from these findings suggests that the last common ancestor of the extant Archaea possessed a complex membrane remodelling apparatus, different components of which were lost during subsequent evolution of archaeal lineages. By contrast, eukaryotes seem to have inherited all three ancest