Assembly of the <i>Caulobacter</i> cell division machine

Goley, Erin D.; Yeh, Yi Chun; Hong, Sun Hae; Fero, M.J.; Abeliuk, Eduardo; McAdams, Harley H.; Shapiro, Lucy

doi:10.1111/j.1365-2958.2011.07677.x

Cited by 134 publications

(224 citation statements)

References 75 publications

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“…A similar pattern is observed in the divisome proteins that are components of the cell-division machine (27). Of 23 divisome proteins, 5 (FzlA, FtsQ, FtsK, FtsL, and FtsB) have this characteristic (worksheet "Divisome Genes" in Dataset S2).…”

Section: Dramatic Cell Cycle-dependent Changes In the Cell's Proteinsupporting

confidence: 59%

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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Section: Dramatic Cell Cycle-dependent Changes In the Cell's Proteinsupporting

confidence: 59%

Dynamic translation regulation in Caulobacter cell cycle control

Schrader

Childers

et al. 2016

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

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“…In C. crescentus, early cell-cycle unipolar FtsZ foci have been reported (2), although whether this localization is more than a postdivision remnant of the Z ring has not been resolved. FtsA in C. crescentus, however, is diffuse in the cytoplasm in the first half of the cell cycle, and then localizes to the Z ring until septation is complete (2).…”

Section: Discussionmentioning

confidence: 99%

“…After elongation is complete, divisome proteins assemble at the midcell in a specific temporal order where one component recruits the next via protein-protein interactions. A comprehensive study in the α-proteobacterium Caulobacter crescentus, however, revealed significant differences from the E. coli model in the timing of localization of cell-division proteins and the genetic requirements for localization (2).…”

mentioning

confidence: 98%

Dynamic FtsA and FtsZ localization and outer membrane alterations during polar growth and cell division in Agrobacterium tumefaciens

Zupan

Cameron

Anderson-Furgeson

et al. 2013

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

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Growth and cell division in rod-shaped bacteria have been primarily studied in species that grow predominantly by peptidoglycan (PG) synthesis along the length of the cell. Rhizobiales species, however, predominantly grow by PG synthesis at a single pole. Here we characterize the dynamic localization of several Agrobacterium tumefaciens components during the cell cycle. First, the lipophilic dye FM 4-64 predominantly stains the outer membranes of old poles versus growing poles. In cells about to divide, however, both poles are equally labeled with FM 4-64, but the constriction site is not. Second, the cell-division protein FtsA alternates from unipolar foci in the shortest cells to unipolar and midcell localization in cells of intermediate length, to strictly midcell localization in the longest cells undergoing septation. Third, the cell division protein FtsZ localizes in a cell-cycle pattern similar to, but more complex than, FtsA. Finally, because PG synthesis is spatially and temporally regulated during the cell cycle, we treated cells with sublethal concentrations of carbenicillin (Cb) to assess the role of penicillin-binding proteins in growth and cell division. Cb-treated cells formed midcell circumferential bulges, suggesting that interrupted PG synthesis destabilizes the septum. Midcell bulges contained bands or foci of FtsA-GFP and FtsZ-GFP and no FM 4-64 label, as in untreated cells. There were no abnormal morphologies at the growth poles in Cb-treated cells, suggesting unipolar growth uses Cb-insensitive PG synthesis enzymes.agrobacterium cell cycle | bacterial cell growth | bacterial cell division | peptidoglycan synthesis

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“…It is expected that the process will be significantly different among microbes: many subunits are not ubiquitously conserved, cytoskeletal elements can vary in structure and function (14), recruitment hierarchy is different even in organisms with conserved subunits (15), and niche-specific regulators of PG growth and interchangeability of enzymatic components seem to be prevalent (4,10). Mapping the differences and also linking them to the physiology of diverse organisms will be in the core of future studies in the field and will help us dissect the general underlying principles of these machineries from the nichespecific ones.…”

mentioning

confidence: 99%