Binary or non-binary fission? Reproductive mode of a predatory bacterium depends on prey size

Abstract

Most eukaryotic and bacterial cells divide by binary fission, where one mother cell produces two progeny cells, or, rarely, by non-binary fission. All bacteria studied to date use only one of these two reproduction modes. Here, we demonstrate for the first time that the predatory bacterium Bdellovibrio bacteriovorus reproduces through both binary and non-binary fission. Switching between the two modes correlates with the prey size. In relatively small host cells, B. bacteriovorus undergoes binary fission; the FtsZ ring assembles in the midcell and the mother cell splits into two daughter cells. In larger host cells, B. bacteriovorus switches to non-binary fission and creates multiple FtsZ rings to produce three or more daughter cells. Completion of bacterial cell cycle critically depends on precise spatiotemporal coordination of chromosome replication and segregation with other cell-cycle events, including cell division. Our studies reveal that B. bacteriovorus always initiates chromosome replication at the invasive pole of the cell, but the spatiotemporal choreography of subsequent steps depends on the fission mode and/or the number of progeny cells. In non-binary dividing filaments producing five or more progeny cells, the last round(s) of replication may also be initiated at the noninvasive pole. Finally, we show that binary-dividing B. bacteriovorus needs to extensively rebuild the flagellated pole of the mother cell to turn it into the invasive pole of a daughter cell. Altogether, we find that B. bacteriovorus reproduces through bimodal fission and that extracellular factors, such as the host size, can shape replication choreography, providing new insights about bacterial life cycles.