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Genes encoding DNA replication proteins have been frequently exchanged between cells and mobile elements, such as viruses or plasmids. This raises potential problems to reconstruct their history. Here, we combine phylogenetic and genomic context analyses to study the evolution of the replicative minichromosome maintenance (MCM) helicases in Archaea. Several archaeal genomes encode more than one copy of the mcm gene. Genome context analysis reveals that most of these additional copies are encoded within mobile elements. Exhaustive analysis of these elements reveals diverse groups of integrated archaeal plasmids or viruses, including several head-and-tail proviruses. Some MCMs encoded by mobile elements are structurally distinct from their cellular counterparts, with one case of novel domain organization. Both genome context and phylogenetic analysis indicate that MCM encoded by mobile elements were recruited from cellular genomes. An accelerated evolution and a dramatic expansion of methanococcal MCMs suggest a host-to-virus-to-host transfer loop, possibly triggered by the loss of the archaeal initiator protein Cdc6 in Methanococcales. Surprisingly, despite extensive transfer of mcm genes between viruses, plasmids, and cells, the topology of the MCM tree is strikingly congruent with the consensus archaeal phylogeny, indicating that mobile elements encoding mcm have coevolved with their hosts and that DNA replication proteins can be also useful to reconstruct the history of the archaeal domain.

The Evolutionary History of Archaeal MCM Helicases: A Case Study of Vertical Evolution Combined with Hitchhiking of Mobile Genetic Elements