Abstract
The bacterial cell cycle has been extensively studied under standard growth conditions. How it is modulated in response to environmental changes remains poorly understood. Here, we demonstrate that the freshwater bacterium Caulobacter crescentus blocks cell division and grows to filamentous cells in response to stress conditions affecting the cell membrane. Our data suggest that stress switches the membrane-bound cell cycle kinase CckA to its phosphatase mode, leading to the rapid dephosphorylation, inactivation and proteolysis of the master cell cycle regulator CtrA. The clearance of CtrA results in downregulation of division and morphogenesis genes and consequently a cell division block. Upon shift to non-stress conditions, cells quickly restart cell division and return to normal cell size. Our data indicate that the temporary inhibition of cell division through the regulated inactivation of CtrA constitutes a growth advantage under stress. Taken together, our work reveals a new mechanism that allows bacteria to alter their mode of proliferation in response to environmental cues by controlling the activity of a master cell cycle transcription factor. Furthermore, our results highlight the role of a bifunctional kinase in this process that integrates the cell cycle with environmental information.
Highlights
The bacterial cell cycle has been studied extensively in the past
Consistent with the flow cytometry data, we found by using a fluorescent repressor-operator system (FROS), which fluorescently marks the origins of replication [31], that the elongated cells contained multiple well-segregated origins (S1 Fig), demonstrating that cells continue to undergo DNA replication, chromosome segregation and cellular growth under these conditions, but that they stop dividing
The effects on cell division were observed within two hours of NaCl or EtOH treatment, the phenotype became more pronounced over time (Fig 1B)
Summary
Biochemistry and more recently, advanced microscopy techniques have provided important insight into the processes of DNA replication, chromosome segregation and cell division, and numerous regulatory mechanisms have been identified that precisely coordinate these processes in time and space. In nature bacteria are exposed to drastic environmental changes, where they have to constantly adjust their growth rate and mode of proliferation [1,2]. It has frequently been reported that various bacteria transform into multi-chromosome containing filaments in response to certain environmental conditions [2,3,4], indicating that bacteria dynamically modulate cell division and the cell cycle in response to environmental cues. The precise mechanisms transducing environmental information into the cell division machinery and how these mechanisms help cells to survive under adverse conditions are not well understood
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