In contrast to the cell division machineries of bacteria, euryarchaea, and eukaryotes, no division components have been identified in the second main archaeal phylum, Crenarchaeota. Here, we demonstrate that a three-gene operon, cdv, in the crenarchaeon Sulfolobus acidocaldarius, forms part of a unique cell division machinery. The operon is induced at the onset of genome segregation and division, and the Cdv proteins then polymerize between segregating nucleoids and persist throughout cell division, forming a successively smaller structure during constriction. The cdv operon is dramatically down-regulated after UV irradiation, indicating division inhibition in response to DNA damage, reminiscent of eukaryotic checkpoint systems. The cdv genes exhibit a complementary phylogenetic range relative to FtsZ-based archaeal division systems such that, in most archaeal lineages, either one or the other system is present. Two of the Cdv proteins, CdvB and CdvC, display homology to components of the eukaryotic ESCRT-III sorting complex involved in budding of luminal vesicles and HIV-1 virion release, suggesting mechanistic similarities and a common evolutionary origin.he Archaea constitute a separate domain of life that has evolved in parallel with Bacteria and Eukarya (1). The archaeal domain is currently divided into two main lineages, the Crenarchaeota and the Euryarchaeota, each of which comprises several distinct classes of organisms that thrive in a wide variety of environments. Whereas several aspects of archaeal biology appear to be unique, certain traits resemble those in eukaryotes, including the machineries that govern information storage, maintenance, and processing.Several features of archaeal cell cycle progression have been elucidated in considerable detail including the overall organization of the cell cycle in certain species, and regulatory and mechanistic aspects of the replication process (2, 3). Conversely, the genome segregation machinery remains essentially uncharacterized in this domain. In archaeal species belonging to the Euryarchaeota phylum, and in bacteria, cell division is mediated by FtsZ protein filaments that form a constricting ring structure (4). In eukaryotes, division occurs with the help of a contractile actin-myosin ring or, in plant cells, by septum formation at a site initially marked by actin and microtubules (5). In contrast to bacteria, euryarchaea, and eukaryotes, no cell division components have been identified in the second main archaeal phylum, Crenarchaeota (2).Here, we report on the identification of key components of the cell division system in the hyperthermophilic crenarchaeon Sulfolobus acidocaldarius, describe intracellular structures that are formed by the gene products during genome segregation and division, and show that the operon is subject to a checkpoint-like regulation. We also demonstrate that the division machinery is present in all crenarchaeal orders except Thermoproteales, and that it is related to the eukaryotic ESCRT-III sorting complex.