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The halophilic archaeon  Haloferax volcanii  has a multireplicon genome, consisting of a main chromosome, three secondary chromosomes, and a plasmid. Genes for the initiator protein Cdc6/Orc1, which are commonly located adjacent to archaeal origins of DNA replication, are found on all replicons except plasmid pHV2. However, prediction of DNA replication origins in  H. volcanii  is complicated by the fact that this species has no less than 14  cdc6/orc1  genes. We have used a combination of genetic, biochemical, and bioinformatic approaches to map DNA replication origins in  H. volcanii.  Five autonomously replicating sequences were found adjacent to  cdc6/orc1  genes and replication initiation point mapping was used to confirm that these sequences function as bidirectional DNA replication origins in vivo. Pulsed field gel analyses revealed that  cdc6/orc1 -associated replication origins are distributed not only on the main chromosome (2.9 Mb) but also on pHV1 (86 kb), pHV3 (442 kb), and pHV4 (690 kb) replicons. Gene inactivation studies indicate that linkage of the initiator gene to the origin is not required for replication initiation, and genetic tests with autonomously replicating plasmids suggest that the origin located on pHV1 and pHV4 may be dominant to the principal chromosomal origin. The replication origins we have identified appear to show a functional hierarchy or differential usage, which might reflect the different replication requirements of their respective chromosomes. We propose that duplication of  H. volcanii  replication origins was a prerequisite for the multireplicon structure of this genome, and that this might provide a means for chromosome-specific replication control under certain growth conditions. Our observations also suggest that  H. volcanii  is an ideal organism for studying how replication of four replicons is regulated in the context of the archaeal cell cycle.

Genetic and Physical Mapping of DNA Replication Origins in Haloferax volcanii