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In this review we stress the differences between eukaryotes and bacteria with respect to their different cell cycles, replication mechanisms and genome organizations. One of the most basic and underappreciated differences is that a bacterial chromosome uses only one  ori  while eukaryotic chromosome uses multiple  oris . Consequently, eukaryotic  ori s work redundantly in a cell cycle divided into separate phases: First inactive replication proteins assemble on eukaryotic  ori s, and then they await conditions (in the separate “S-phase”) that activate only the  ori -bound and pre-assembled replication proteins. S-phase activation (without re-assembly) ensures that a eukaryotic  ori  “fires” (starts replication) only once and that each chromosome consistently duplicates only once per cell cycle. This precise chromosome duplication does not require precise multiple  ori  firing in S-phase. A eukaryotic  ori  can fire early, late or not at all. The single bacterial  ori  has no such margin for error and a comparable imprecision is lethal. Single  ori  usage is not more primitive; it is a totally different strategy that distinguishes bacteria. We further argue that strong evolutionary pressures created more sophisticated single  ori  systems because bacteria experience extreme and rapidly changing conditions. A bacterial  ori  must rapidly receive and process much information in “real-time” and not just in “cell cycle time.” This redefinition of bacterial  oris  as centralized information processors makes at least two important predictions: First that bacterial  oris  use many and yet to be discovered control mechanisms and second that evolutionarily distinct bacteria will use many very distinct control mechanisms. We review recent literature that supports both predictions. We will highlight three key examples and describe how negative-feedback, phospho-relay, and chromosome-partitioning systems act to regulate chromosome replication. We also suggest future studies and discuss using replication proteins as novel antibiotic targets.

Redefining bacterial origins of replication as centralized information processors