The Genetic Basis of Laboratory Adaptation in
            <i>Caulobacter crescentus</i>

Marks, Melissa E.; Castro-Rojas, Cyd Marie; Teiling, Clotilde; Du, Lei; Kapatral, Vinayak; Walunas, Theresa L.; Crosson, Sean

doi:10.1128/jb.00255-10

Cited by 176 publications

(190 citation statements)

References 41 publications

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“…1) that implement biogenesis of polar organelles, replication and segregation of the chromosome, and cytokinesis (1)(2)(3)(4). The circular 4-Mb genome has 3,885 ORFs and 199 noncoding RNAs (5,6). mRNA profiling by microarrays or RNA-seq (7)(8)(9)(10) and global promoter activity profiles from 5′ Global RACE experiments (11) have shown that several hundred Caulobacter mRNAs have significant temporal transcriptional variation over the cell cycle.…”

mentioning

confidence: 99%

Dynamic translation regulation in Caulobacter cell cycle control

Schrader

Childers

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Progression of the Caulobacter cell cycle requires temporal and spatial control of gene expression, culminating in an asymmetric cell division yielding distinct daughter cells. To explore the contribution of translational control, RNA-seq and ribosome profiling were used to assay global transcription and translation levels of individual genes at six times over the cell cycle. Translational efficiency (TE) was used as a metric for the relative rate of protein production from each mRNA. TE profiles with similar cell cycle patterns were found across multiple clusters of genes, including those in operons or in subsets of operons. Collections of genes associated with central cell cycle functional modules (e.g., biosynthesis of stalk, flagellum, or chemotaxis machinery) have consistent but different TE temporal patterns, independent of their operon organization. Differential translation of operon-encoded genes facilitates precise cell cycle-timing for the dynamic assembly of multiprotein complexes, such as the flagellum and the stalk and the correct positioning of regulatory proteins to specific cell poles. The cell cycleregulatory pathways that produce specific temporal TE patterns are separate from-but highly coordinated with-the transcriptional cell cycle circuitry, suggesting that the scheduling of translational regulation is organized by the same cyclical regulatory circuit that directs the transcriptional control of the Caulobacter cell cycle.T he Caulobacter crescentus cell cycle produces two daughter cell types at each cell division: a nonreplicative motile swarmer cell, and a replication-competent sessile stalked cell. At the time of the asymmetric cell division, each daughter cell activates a different genetic program. Caulobacter has a cyclical genetic circuit that controls the varying temporal and spatial expression of multiple functional modules (Fig. 1) that implement biogenesis of polar organelles, replication and segregation of the chromosome, and cytokinesis (1-4). The circular 4-Mb genome has 3,885 ORFs and 199 noncoding RNAs (5, 6). mRNA profiling by microarrays or RNA-seq (7-10) and global promoter activity profiles from 5′ Global RACE experiments (11) have shown that several hundred Caulobacter mRNAs have significant temporal transcriptional variation over the cell cycle. The expression of cell cycle-controlled mRNAs largely correlates with the times they are required for the functional modules that implement progression of the cell cycle (8). The transcriptional activity of most of the Caulobacter cell cycle-regulated promoters is controlled by a genetic circuit comprised of four transcriptional master regulators, a DNA methyltransferase (2), and a dynamic set of polar-localized phospho-signaling proteins that control asymmetric cell division (12-15). Because regulation of translation has an immediate impact on protein production, a major cellular energy drain, tight regulation of translation is essential for rapid cell adaptation to changing circumstances. In eukaryotic cells translational contr...

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confidence: 99%

Dynamic translation regulation in Caulobacter cell cycle control

Schrader

Childers

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…The CB15N WT C. crescentus strain, used in this study, is a strain that adapted to laboratory growth conditions and lost its ability to attach to surfaces. For more information on this strain, see (36).…”

Section: Experimental Procedures Bacterial Strains Media and Plasmidsmentioning

confidence: 99%

An essential thioredoxin is involved in the control of the cell cycle in the bacterium Caulobacter crescentus

Goemans

Beaufay

Wahni

et al. 2018

Journal of Biological Chemistry

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Thioredoxins (Trxs) are antioxidant proteins that are conserved among all species. These proteins have been extensively studied and perform reducing reactions on a broad range of substrates. Here, we identified Caulobacter crescentus Trx1 (CCNA_03653; CcTrx1) as an oxidoreductase that is involved in the cell cycle progression of this model bacterium and is required to sustain life. Intriguingly, the abundance of CcTrx1 varies throughout the C. crescentus cell cycle: while the expression of CcTrx1 is induced in stalked cells, right before DNA replication initiation, CcTrx1 is actively degraded by the ClpXP protease in predivisional cells. Importantly, we demonstrated that regulation of the abundance of CcTrx1 is crucial for cell growth and survival as modulating CcTrx1 levels leads to cell death. Finally, we also report a comprehensive biochemical and structural characterization of this unique and essential Trx. The requirement to precisely control the abundance of CcTrx1 for cell survival underlines the importance of redox control for optimal cell cycle progression in C. crescentus. INTRODUCTIONThioredoxins (Trx) are small antioxidant proteins that have been identified in most living organisms. They receive electrons from NADPH through the flavoprotein thioredoxin reductase and catalyze the reduction of oxidized cysteine residues in substrate proteins (1). As such, they are implicated in a variety of processes, ranging from oxidative stress defense to signal transduction. These soluble proteins all share a similar structure, a Trx-fold consisting of five b-strands surrounded by 4 ahelices. They also display a strictly conserved WCGPC catalytic active site motif and contain a cis-proline residue (1). The two cysteines of the catalytic motif are the key players involved in the reduction of oxidized substrates.First identified in 1964 as an electron donor for ribonucleotide reductase (2,3), Escherichia coli Trx1 (EcTrx1) is a major http://www.jbc.org/cgi

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“…The presence of these genes could alter the capsular properties of C. crescentus, and as a consequence interfere with phage ΦCr30 attachment to the S-layer. Moreover, the presence of a modified capsule on the cell surface might affect the cell density and hydrodynamic properties, which in turn would be responsible for the change in the sedimentation properties (127).…”

Section: Regulation Of Mucoidy and Cell Densitymentioning

confidence: 99%

“…These NA1000 distinctive phenotypes include the mucoidy on high-sugar medium, a reduced sensitivity to phage ΦCr30 and the sedimentation properties which are exploited to physically separate swarmer and stalked cells by cell density centrifugation (127). The 26-kb prophage region encodes a number of putative ORFs predicted to be involved in polysaccharide synthesis and export (127). The presence of these genes could alter the capsular properties of C. crescentus, and as a consequence interfere with phage ΦCr30 attachment to the S-layer.…”

Section: Regulation Of Mucoidy and Cell Densitymentioning

confidence: 99%

Developmental and environmental regulatory pathways in alpha-proteobacteria

Ardissone

Viollier²

2012

Front Biosci

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Spatial and temporal control of cell differentiation and morphogenesis plays a key role in prokaryotes as well as eukaryotes. This is particularly important for bacteria that divide asymmetrically, as they generate two morphologically and functionally distinct daughter cells. Several alpha-proteobacteria, including the aquatic, free-living Caulobacter crescentus, the symbiotic rhizobia and the plant and animal pathogens Agrobacterium and Brucella, have been shown to undergo asymmetrical division. C. crescentus has become a model system for the study of the regulatory networks, in particular the control of the cell cycle, the cytokinetic machinery, the cytoskeleton and the functions required for duplication and differentiation in general. As the bulk of these regulatory networks and functions is conserved in most alpha-proteobacteria, we recapitulate the recent advances in understanding these spatially and temporally controlled processes, focusing on cell cycle progression, DNA replication and partitioning, cell division and regulation of specific phenotypes that vary during the cell cycle or in the case of different lifestyles (like extracellular polysaccharide production) in C. crescentus and other alpha-proteobacteria

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The Genetic Basis of Laboratory Adaptation in Caulobacter crescentus

Cited by 176 publications

References 41 publications

Dynamic translation regulation in Caulobacter cell cycle control

Dynamic translation regulation in Caulobacter cell cycle control

An essential thioredoxin is involved in the control of the cell cycle in the bacterium Caulobacter crescentus

Developmental and environmental regulatory pathways in alpha-proteobacteria

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