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Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus

Nature Reviews Microbiology volume 2, pages 325–337 (2004)Cite this article

Key Points

  • Progression through the cell cycle requires the precise coordination of four important processes: DNA replication, chromosome segregation, cell division and cell growth. The aquatic, non-pathogenic bacterium Caulobacter crescentus has emerged as the main model system for analysis of the prokaryotic cell cycle.

  • In contrast to many other prokaryotes, including Escherichia coli, Caulobacter cells, like most eukaryotes, exhibit strict once-and-only-once replication of the chromosome. Cell division yields two daughter cells that are physiologically and morphologically different. One daughter cell is a stalked cell that immediately reinitiates another round of chromosome replication, whereas the other daughter cell is a swarmer cell that cannot start DNA replication until after an obligate swarmer-to-stalked cell differentiation step.

  • The use of transcriptome analysis, together with proteome analysis, to define the genes and products that are crucial for cell-cycle progression and generation and maintenance of asymmetry is described. These studies have confirmed and extended the array of genes involved in cell cycle regulation previously identified using genetic and biochemical techniques.

  • CtrA is a master regulatory protein that controls key cell-cycle events. The CtrA regulon has been mapped out — 26% of all cell-cycle-regulated genes are controlled by CtrA. The mechanisms of regulation of CtrA itself are discussed, including control of CtrA transcription, phosphorylation, proteolysis and compartmentalization.

  • The authors discuss what is meant by a cell-cycle checkpoint and review evidence for whether Caulobacter has a dedicated checkpoint system.

  • Finally, mechanisms by which Caulobacter couples morphological transitions and gene expression are described together with the future directions for research using this outstanding model system.

Abstract

Microorganisms make tractable model systems and Caulobacter crescentus has emerged as the main model for understanding the regulation of the bacterial cell cycle. Mechanisms that mediate the generation and maintenance of spatial asymmetry are being uncovered using this model bacterium. Now, the advent of genomic technologies together with the completion of the Caulobacter crescentus genome sequence is enabling global analyses that have revolutionized the pace of research into the genetic networks that control the bacterial life cycle.

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Figure 1: Cell-cycle progression in Caulobacter crescentus.
Figure 2: Transcriptional control of flagellar assembly.
Figure 3: Regulation of the master regulator CtrA.
Figure 4: Phosphorylation of the essential response regulators CtrA and DivK.
Figure 5: CtrA regulon.
Figure 6: Strategies for coupling-dependent processes.
Figure 7: Subcellular localization and cellular asymmetry.

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Acknowledgements

We apologize to our colleagues whose work was not cited owing to space constraints. We thank L. Garwin and A. Greenwood for helpful comments on the manuscript. Work in the Laub laboratory is supported by the Office of Science (BER), US Department of Energy, the National Institutes of Health and the Defense Advanced Research Projects Agency.

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Authors and Affiliations

  1. Bauer Center for Genomics Research, 7 Divinity Avenue, Cambridge, 02138, Massachusetts, USA

    Jeffrey M. Skerker & Michael T. Laub

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  1. Jeffrey M. Skerker
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Correspondence to Michael T. Laub.

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DATABASES

Entrez

Agrobacterium tumefaciens

Caulobacter crescentus

Escherichia coli

Pseudomonas aeruginosa

Rickettsia prowazekii

Sinorhizobium meliloti

SwissProt

CckA

CpaC

CpaE

CtrA

DivJ

DivK

DivL

FlbD

FliX

FtsZ

PleC

PodJ

Spo0A

Spo0F

Glossary

G1 PHASE

The period of time in the cell cycle before DNA replication starts and during which the cell contains only one copy of its genome.

S PHASE

The period of time in the cell cycle in which a cell is actively synthesizing/replicating its genome.

G2 PHASE

The period of time in the cell cycle after DNA replication has been completed, but before cell division.

PULSE–CHASE STUDY

A technique in which a cell, or cell extract, is briefly treated with a radioactive compound (the 'pulse'). This allows incorporation of the radiolabel into cellular constituents. The pulse is followed by addition of excess, non-radioactive compound (the 'chase'). Monitoring the radiolabelled compound over time then allows its location or stability to be tracked.

DNA METHYLATION

The addition of a methyl (CH3) group to adenine or cytosine bases in DNA.

HOMOLOGY MODELLING

A procedure in which an unknown protein structure is modelled by matching — fitting — to the known structure of a closely related protein by matching conserved amino acids. Allows an approximation of the 3D shape and organization of the protein to be obtained.

MULTI-COMPONENT PHOSPHORELAY

A signalling pathway involving two-component signal transduction molecules, in which a phosphoryl group from ATP is transferred to more than two components. Usually involves transfer from a histidine kinase to a response regulator to a histidine phosphotransferase to another response regulator.

CLOSED-LOOP SET

A set of regulatory factors that regulate each other such that the overall topology produces a circle, or loop, of interactions.

NASCENT SWARMER POLE

The pole opposite the stalked pole in a Caulobacter predivisional cell, where the flagellum and pilus secretion apparatus must be assembled before cell division takes place.

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Skerker, J., Laub, M. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2, 325–337 (2004). https://doi.org/10.1038/nrmicro864

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