Comparative analysis of Caulobacter chromosome replication origins

Shaheen, S‐M; Ouimet, Marie-Claude; Marczynski, Gregory T.

doi:10.1099/mic.0.025528-0

Cited by 32 publications

(41 citation statements)

References 39 publications

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“…In addition, putative CtrA-binding sites were identified in the origin of replication (Fig. 4C), suggesting a role for CtrA in integrating DNA replication with the cell cycle, as described for Caulobacter species (55,56). Further support for the hypothesis that DNA replication is integrated with the P. hirschii cell cycle was provided by the presence of four consensus CcrM methylation sites (GANTC [7]) (Fig.…”

Section: Resultsmentioning

confidence: 53%

Short-Stalked Prosthecomicrobium hirschii Cells Have a Caulobacter-Like Cell Cycle

et al. 2016

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The dimorphic alphaproteobacterium Prosthecomicrobium hirschii has both short-stalked and long-stalked morphotypes. Notably, these morphologies do not arise from transitions in a cell cycle. Instead, the maternal cell morphology is typically reproduced in daughter cells, which results in microcolonies of a single cell type. In this work, we further characterized the shortstalked cells and found that these cells have a Caulobacter-like life cycle in which cell division leads to the generation of two morphologically distinct daughter cells. Using a microfluidic device and total internal reflection fluorescence (TIRF) microscopy, we observed that motile short-stalked cells attach to a surface by means of a polar adhesin. Cells attached at their poles elongate and ultimately release motile daughter cells. Robust biofilm growth occurs in the microfluidic device, enabling the collection of synchronous motile cells and downstream analysis of cell growth and attachment. Analysis of a draft P. hirschii genome sequence indicates the presence of CtrA-dependent cell cycle regulation. This characterization of P. hirschii will enable future studies on the mechanisms underlying complex morphologies and polymorphic cell cycles. IMPORTANCEBacterial cell shape plays a critical role in regulating important behaviors, such as attachment to surfaces, motility, predation, and cellular differentiation; however, most studies on these behaviors focus on bacteria with relatively simple morphologies, such as rods and spheres. Notably, complex morphologies abound throughout the bacteria, with striking examples, such as P. hirschii, found within the stalked Alphaproteobacteria. P. hirschii is an outstanding candidate for studies of complex morphology generation and polymorphic cell cycles. Here, the cell cycle and genome of P. hirschii are characterized. This work sets the stage for future studies of the impact of complex cell shapes on bacterial behaviors. The Alphaproteobacteria comprise a diverse group of bacteria, including important pathogens of animals (Brucella spp. and Rickettsia spp.) and plants (Agrobacterium spp.), plant symbionts (Rhizobium spp., Sinorhizobium spp., and Mesorhizobium spp.), photosynthetic bacteria (Rhodobacter spp.), freshwater bacteria (Caulobacter spp.), and marine bacteria (Hyphomonas spp.). Despite the diverse habitats and lifestyles of these bacteria, many alphaproteobacterial species have a characteristic life cycle that culminates in asymmetric cell division (1-4). Caulobacter crescentus has served as a model bacterial system for the study of cell cycle regulation, and decades of research have provided insights into the mechanism underlying the precise cell cycle control that allows

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Section: Resultsmentioning

confidence: 53%

Short-Stalked Prosthecomicrobium hirschii Cells Have a Caulobacter-Like Cell Cycle

et al. 2016

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“…CtrA is a global response regulator protein that binds to and represses the C. crescentus origin of chromosome replication in the swarmer cells (10,(14)(15)(16). Competitive binding between CtrA and DnaA is a key mechanism of replication control that blocks replication in swarmer cells while allowing replication in the stalked cells (10,17). In addition to this dimorphic control, C. crescentus chromosome replication occurs once and only once per cell division cycle (18).…”

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confidence: 99%

The Caulobacter crescentus Homolog of DnaA (HdaA) Also Regulates the Proteolysis of the Replication Initiator Protein DnaA

Wargachuk

Marczynski

2015

J Bacteriol

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It is not known how diverse bacteria regulate chromosome replication. Based on Escherichia coli studies, DnaA initiates replication and the homolog of DnaA (Hda) inactivates DnaA using the RIDA (regulatory inactivation of DnaA) mechanism that thereby prevents extra chromosome replication cycles. RIDA may be widespread, because the distantly related Caulobacter crescentus homolog HdaA also prevents extra chromosome replication (J. While most bacteria use the DnaA protein to initiate chromosome replication (1-3), bacteria responding to diverse environmental pressures probably evolved many different mechanisms to regulate DnaA and thereby adjust replication control to their specific needs (3-5). The model Gram-negative bacterium Caulobacter crescentus is found in nutrient-poor freshwater lakes and streams (6). C. crescentus evolved to divide asymmetrically, and it produces a motile "swarmer cell" and a nonmotile "stalked cell" after each cell division (6-8). Chromosome replication is coupled to this dimorphic cell division since only the stalked cells initiate chromosome replication, and the swarmer cells differentiate into stalked cells before they replicate their chromosomes (9-13). CtrA is a global response regulator protein that binds to and represses the C. crescentus origin of chromosome replication in the swarmer cells (10,(14)(15)(16). Competitive binding between CtrA and DnaA is a key mechanism of replication control that blocks replication in swarmer cells while allowing replication in the stalked cells (10,17). In addition to this dimorphic control, C. crescentus chromosome replication occurs once and only once per cell division cycle (18). However, CtrA activity does not block extra rounds of chromosome replication prior to cell division (16,19).Escherichia coli uses at least three mechanisms to block extra rounds of chromosome replication. As reviewed by Katayama and coworkers (20), E. coli possesses two mechanisms that restrict DnaA binding to the origin of replication (oriC) and one mechanism, termed RIDA (regulatory inactivation of DnaA), that inactivates DnaA. Of these three mechanisms, RIDA is the dominant mechanism in E. coli (20,21). E. coli DnaA binds ATP or ADP, but only the active DnaA-ATP form can initiate oriC replication. RIDA prevents overreplication by producing the inactive DnaA-ADP form. This is essentially a negative-feedback mechanism that Citation Wargachuk R, Marczynski GT. 2015. The Caulobacter crescentus homolog of DnaA (HdaA) also regulates the proteolysis of the replication initiator protein DnaA.

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“…Yet, how exactly does methylation make the chromosome competent for replication? One possibility is that it is due to remethylation of the CcrM recognition sites in the Cori, similar to the situation in E. coli, where the SeqA protein recognizes hemimethylated sites in the ori and sequesters them from replication until they are remethylated (21,227 (216). It seems likely that methylation regulates replication competence in a different fashion.…”

Section: Regulation Of Dna Replication and Methylation Machinerymentioning

confidence: 98%

“…Specifically, the A and B sites work cooperatively to block P s activity, site C overlaps the IHF binding site, and site E overlaps a DnaA box (199,220,221). Comparison of freshwater and marine Caulobacter oris demonstrates that while the number and position of CtrA binding sites are variable, the most conserved CtrA binding sites are always found in close proximity to DnaA binding sites, indicating that the most universally conserved function of CtrA in the ori is to modulate DnaA binding and subsequent replication initiation (216). This result underscores the importance of CtrA inhibiting replication.…”

Section: The Origin Of Replicationmentioning

confidence: 99%

Getting in the Loop: Regulation of Development inCaulobacter crescentus

Curtis

Brun

2010

Microbiol Mol Biol Rev

244

233

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SUMMARY Caulobacter crescentus is an aquatic Gram-negative alphaproteobacterium that undergoes multiple changes in cell shape, organelle production, subcellular distribution of proteins, and intracellular signaling throughout its life cycle. Over 40 years of research has been dedicated to this organism and its developmental life cycles. Here we review a portion of many developmental processes, with particular emphasis on how multiple processes are integrated and coordinated both spatially and temporally. While much has been discovered about Caulobacter crescentus development, areas of potential future research are also highlighted.

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Comparative analysis of Caulobacter chromosome replication origins

Cited by 32 publications

References 39 publications

Short-Stalked Prosthecomicrobium hirschii Cells Have a Caulobacter-Like Cell Cycle

Short-Stalked Prosthecomicrobium hirschii Cells Have a Caulobacter-Like Cell Cycle

The Caulobacter crescentus Homolog of DnaA (HdaA) Also Regulates the Proteolysis of the Replication Initiator Protein DnaA

Getting in the Loop: Regulation of Development inCaulobacter crescentus

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