Regulatory Response to Carbon Starvation in Caulobacter crescentus

Britos, Leticia; Abeliuk, Eduardo; Taverner, Thomas; Lipton, Mary; McAdams, Harley H.; Shapiro, Lucy

doi:10.1371/journal.pone.0018179

Cited by 69 publications

(88 citation statements)

References 75 publications

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“…Cells were collected at the indicated times for immunoblot analysis using antibodies raised against CtrA. sigma factor might activate the proteolysis of CtrA in response to carbon starvation (17). Our results suggest that the degradation of CtrA during starvation is not a consequence of (p)ppGpp accumulation, but rather a consequence of a more general stress response that may involve SigT, since CtrA is stabilized rather than destabilized by (p)ppGpp in nonstarved cells.…”

Section: Resultsmentioning

confidence: 78%

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Effects of (p)ppGpp on the Progression of the Cell Cycle of Caulobacter crescentus

González

Collier

2014

J Bacteriol

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Bacteria must control the progression of their cell cycle in response to nutrient availability. This regulation can be mediated by guanosine tetra-or pentaphosphate [(p)ppGpp], which are synthesized by enzymes of the RelA/SpoT homologue (Rsh) family, particularly under starvation conditions. Here, we study the effects of (p)ppGpp on the cell cycle of Caulobacter crescentus, an oligotrophic bacterium with a dimorphic life cycle. C. crescentus divides asymmetrically, producing a motile swarmer cell that cannot replicate its chromosome and a sessile stalked cell that is replication competent. The swarmer cell rapidly differentiates into a stalked cell in appropriate conditions. An artificial increase in the levels of (p)ppGpp in nonstarved C. crescentus cells was achieved by expressing a truncated relA gene from Escherichia coli, encoding a constitutively active (p)ppGpp synthetase. By combining single-cell microscopy, flow cytometry approaches, and swarming assays, we show that an increase in the intracellular concentration of (p)ppGpp is sufficient to slow down the swarmer-to-stalked cell differentiation process and to delay the initiation of chromosome replication. We also present evidence that the intracellular levels of two master regulators of the cell cycle of C. crescentus, DnaA and CtrA, are modulated in response to (p)ppGpp accumulation, even in the absence of actual starvation. CtrA proteolysis and DnaA synthesis seem indirectly inhibited by (p)ppGpp accumulation. By extending the life span of the motile nonreproductive swarmer cell and thus promoting dispersal and foraging functions over multiplication under starvation conditions, (p)ppGpp may play a central role in the ecological adaptation of C. crescentus to nutritional stresses.

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Section: Resultsmentioning

confidence: 78%

“…When C. crescentus swarmer cells are starved for carbon or nitrogen, the swarmer-to-stalked cell transition is delayed or blocked for a subset of the cells in the population (16)(17)(18). In addition, the G 1 -to-S phase transition is blocked in a large majority of the cells (16)(17)(18)(19).…”

mentioning

confidence: 99%

Effects of (p)ppGpp on the Progression of the Cell Cycle of Caulobacter crescentus

González

Collier

2014

J Bacteriol

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“…Stalk development and replication initiation appear largely coupled during glucose exhaustion as well. Different results were observed in experiments in which glucose was completely removed: cells that are abruptly starved for glucose show small stalks that develop in 65% of swarmer cells after 2 h, even while origins are replicated in only 10% of swarmer cells (5). These disparities may indicate that developmental phenotypes can vary based on specific environmental conditions such as abrupt starvation versus gradual nutrient exhaustion.…”

Section: Resultsmentioning

confidence: 79%

“…The stalked and swarmer bands were put into separate tubes and washed in M2. For Western blot samples in replete medium, synchronies were conducted as described previously (5). Cultures for Western blot samples during glucose exhaustion were grown in M2G, pelleted, resuspended in M2G 1/10 at an OD 660 of 0.13, shaken at 30°C until they reached an OD 660 of 0.23, and then pelleted and resuspended in filter-sterilized spent M2G 1/10 medium taken from wild-type cultures that also grew from an OD 660 of 0.13 to an OD 660 of 0.23.…”

Section: Methodsmentioning

confidence: 99%

ppGpp and Polyphosphate Modulate Cell Cycle Progression in Caulobacter crescentus

Boutte

Henry

Crosson

2011

Journal of Bacteriology

113

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Caulobacter crescentus differentiates from a motile, foraging swarmer cell into a sessile, replication-competent stalked cell during its cell cycle. This developmental transition is inhibited by nutrient deprivation to favor the motile swarmer state. We identify two cell cycle regulatory signals, ppGpp and polyphosphate (polyP), that inhibit the swarmer-to-stalked transition in both complex and glucose-exhausted media, thereby increasing the proportion of swarmer cells in mixed culture. Upon depletion of available carbon, swarmer cells lacking the ability to synthesize ppGpp or polyP improperly initiate chromosome replication, proteolyze the replication inhibitor CtrA, localize the cell fate determinant DivJ, and develop polar stalks. Furthermore, we show that swarmer cells produce more ppGpp than stalked cells upon starvation. These results provide evidence that ppGpp and polyP are cell-type-specific developmental regulators.

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“…1B) encoded three genes away from phyR, mediates stress-dependent transcription and cell survival and can phosphorylate PhyR in vivo (25). In C. crescentus, the ortholog of ecfG known as sigT regulates adaptation to osmotic and oxidative stress (2) and carbon limitation (5); nepR and phyR function in the same pathway as sigT (17,25).…”

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confidence: 99%

The LovK-LovR Two-Component System Is a Regulator of the General Stress Pathway in Caulobacter crescentus

2012

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A conserved set of regulators control the general stress response in Caulobacter crescentus , including σ T , its anti-σ factor NepR, the anti-anti-σ factor PhyR, and the transmembrane sensor kinase PhyK. We report that the soluble histidine kinase LovK and the single-domain response regulator LovR also function within the C. crescentus general stress pathway. Our genetic data support a model in which LovK-LovR functions upstream of σ T by controlling the phosphorylation state and thus anti-anti-σ activity of PhyR. Transcription of lovK and lovR is independently activated by stress through a mechanism that requires sigT and phyR . Conversely, lovK and lovR function together to repress transcription of the general stress regulon. Concordant with a functional role of the LovK-LovR two-component system as a negative regulator of the general stress pathway, lovK - lovR -null mutants exhibit increased cell survival after osmotic stress, while coordinate overexpression of lovK and lovR attenuates cell survival relative to that of the wild type. Notably, lovK can complement the transcriptional and cell survival defects of a phyK -null mutant when lovR is deleted. Moreover, in this same genetic background, σ T -dependent transcription is activated in response to osmotic stress. This result suggests that flavin-binding LOV (light, oxygen, or voltage) histidine kinases are competent to perceive cytoplasmic signals in addition to the environmental signal blue light. We conclude that the PhyK-PhyR and LovK-LovR two-component signaling systems coordinately regulate stress physiology in C. crescentus .

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Regulatory Response to Carbon Starvation in Caulobacter crescentus

Cited by 69 publications

References 75 publications

Effects of (p)ppGpp on the Progression of the Cell Cycle of Caulobacter crescentus

Effects of (p)ppGpp on the Progression of the Cell Cycle of Caulobacter crescentus

ppGpp and Polyphosphate Modulate Cell Cycle Progression in Caulobacter crescentus

The LovK-LovR Two-Component System Is a Regulator of the General Stress Pathway in Caulobacter crescentus

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