A Caulobacter gene involved in polar morphogenesis

Driks, Adam; Schoenlein, Patricia V.; DeRosier, David J.; Shapiro, Lucille; Ely, Bert

doi:10.1128/jb.172.4.2113-2123.1990

Cited by 14 publications

(15 citation statements)

References 34 publications

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“…Electron micrographs revealed that the long cells were most often continuous and noncompartmentalized. Another morphological feature of flaS mutant strains was the presence of bifurcated stalks (>25% of the cells in the culture) similar to those seen with flbT mutants (15). In contrast, wild-type C. crescentus rarely (<1%) produces long, undivided cells (Fig.…”

Section: Resultsmentioning

confidence: 66%

“…In contrast, wild-type C. crescentus rarely (<1%) produces long, undivided cells (Fig. 2B), and the occurrence of forked stalks was found to be approximately 1 to 5% (15).…”

Section: Resultsmentioning

confidence: 93%

“…is not required for the transcription of the flaS (56) and the fliLM (55) genes (5 (15) and may represent a general defect affecting the sites of cell division.…”

Section: Discussionmentioning

confidence: 99%

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Expression of an early gene in the flagellar regulatory hierarchy is sensitive to an interruption in DNA replication

et al. 1992

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Genes involved in the biogenesis of the flagellum in Caulobacter crescentus are expressed in a temporal order and are controUed by a trans-acting regulatory hierarchy. Strains with mutations in one of these genes, flaS, cannot transcribe flageUlar structural genes and divide abnormally. This gene was cloned, and it was found that its transcription is initiated early in the cell cycle. Subclones that restored motility toflaS mutants also restored normal cell division. Although transcription offlaS was not dependent on any other known gene in the flagellar hierarchy, it was autoregulated and subject to mild negative control by other genes at the same level of the hierarchy. An additional level of control was revealed when it was found that an interruption of DNA replication caused the inhibition offlaS transcription. TheflaS transcript initiation site was identified, and an apparently unique promoter sequence was found to be highly conserved among the genes at the same level of the hierarchy. The flagellar genes with this conserved 5' region all initiate transcription eariy in the cell cycle and are all sensitive to a disruption in DNA replication. Mutations in these genes also cause an aberrant cell division phenotype. Therefore, flagellar genes at or near the top of the hierarchy may be controlled, in part, by a unique transcription factor and may be responsive to the same DNA replication cues that mediate other cell cycle events, such as cell division.Each Caulobacter crescentus cell division produces morphologically distinct progeny that exhibit different programs of gene expression ( Fig. 1) (14, 23, 40). The progeny stalked cell immediately initiates DNA replication, whereas chromosome replication is delayed in the progeny swarmer cell until its transition to a stalked cell later in the cell cycle (12,34). This transition is marked by the loss of the polar flagellum and initiation of stalk formation at the site previously occupied by the flagellum. Shortly after DNA replication begins, the stalked cell embarks upon the ordered transcription of a group of flagellar genes that culminates in the biogenesis of a new flagellum at the cell pole opposite the stalk.The biogenesis and function of the C. crescentus flagellum require the coordinated expression of at least 48 genes (17). These genes are organized in a trans-acting regulatory hierarchy in which the temporal order of transcription of the structural genes reflects the order of flagellar component assembly (14,23,40). Differential activation of or'4 promoters contributes to the temporal sequence of class II and class III flagellar gene transcription (13,22,24,(37)(38)(39)43) and the localized positioning of flagellar gene products (21,33). An additional level of control was revealed when Newton and coworkers showed that the synthesis of the hook protein and the flagellins is dependent on DNA replication (45)(46)(47)(48)(49)52).

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Section: Resultsmentioning

confidence: 66%

“…In contrast, wild-type C. crescentus rarely (<1%) produces long, undivided cells (Fig. 2B), and the occurrence of forked stalks was found to be approximately 1 to 5% (15).…”

Section: Resultsmentioning

confidence: 93%

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Expression of an early gene in the flagellar regulatory hierarchy is sensitive to an interruption in DNA replication

et al. 1992

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“…The polar organelle has not been identified in all polarly flagellated bacteria, although it is possible that more subtle structures take on a similar role. For example, in C. crescentus, 10-nm-diameter polar particles of unknown function have been observed at the flagellated pole of predivisional cells and occasionally observed in the tips of stalks which are derived from a flagellated pole (18). Nonflagellated cells do not have any polar particles at the cell end.…”

Section: Morphological Differences At Cell Endsmentioning

confidence: 99%

Polarity in Action: Asymmetric Protein Localization in Bacteria

2001

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Recent advances in microscopy and protein localization techniques have provided new insights into the remarkable complexity of the bacterial cell. Although bacteria lack discrete cellular compartments such as organelles, they possess an impressive scheme of subcellular organization at the level of protein localization. There are a growing number of examples of bacterial proteins for which specific intracellular localizations are essential for proper function and regulation. Dynamic polar localization of proteins critical for cell division, chromosome partitioning, and cell cycle control in Escherichia coli, Bacillus subtilis, and Caulobacter crescentus have recently been described (see Table 1). These exciting observations establish that bacterial polarity plays a critical cellular role and that prokaryotic organization is much more complex than previously believed.Clearly, many proteins and protein complexes are able to navigate the bacterial cell and ultimately recognize their appropriate destinations. The current challenge is to uncover the mechanisms, both active and passive, by which proteins are localized and then maintained at the proper intracellular location. The goal of this minireview is to explore a variety of examples of bacterial polarity, to expand upon the current models of polar localization, and to shed light on the spectrum of ways that bacteria may distinguish the polar cellular membrane from the lateral membrane. Several excellent reviews covering recent observations of dynamic polar protein localization have recently been published (7,37,38,41,76,82,83,92,93,102). Here we focus on other aspects of bacterial polarity, including the ultrastructural differences at the cell pole, the modes of polarity in actin-based motility and chemotaxis, and the implications of polarity in bacterial cellular function. MORPHOLOGICAL DIFFERENCES AT CELL ENDSThe diversity of bacterial shapes extends well beyond the basic sphere, rod, and spirochete forms. Many bacteria are decorated with pili, flagella, and/or stalks, which are often found exclusively at one or both cell poles. The presence of such polar structures reveals that at least some bacteria display a complicated organization scheme, since biogenesis of polar structures clearly demands an asymmetry of their components.In addition to these external polar structures, early ultrastructural studies revealed internal differences at the cell poles of some bacteria. One striking example is the polar organelle found at the flagellated pole of diverse gram-negative bacteria such as Aquaspirillum (65), Sphaerotilus (96), Rhodopseudomonas (95), Campylobacter (9, 75), and Helicobacter (63). In each case, the polar organelle is subpolarly located near the cytoplasmic membrane adjacent to the flagella (Fig. 1), suggesting a relationship between the polar flagella and the polar organelle. Further supporting this model, Sphaerotilus natans swarm cells have a polar organelle, whereas nonmotile cells do not (34). The polar organelle has not been identified in all polarl...

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“…Large (90 to 130 nm) disks associated with the outer membrane are another structural component of flagella found thus far only in polarly flagellated bacteria (12,18,22,42,55). These disks might serve to anchor the basal flagellar apparatus or to position the polar flagella (18).…”

Section: Methodsmentioning

confidence: 99%

New structural features of the flagellar base in Salmonella typhimurium revealed by rapid-freeze electron microscopy

Khan

Reese

1991

J Bacteriol

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The structure of the flagellar base in SalmoneUla typhimurium has been studied by rapid-freeze techniques.Freeze-substituted thin sections and freeze-etched replicas of cell envelope preparations have provided complementary information about the flagellar base. The flagellar base has a bell-shaped extension reaching as far as 50 nm into the bacterial cytoplasm. This structure can be recognized in intact bacteria but was studied in detail in cell envelopes, where some flagella lacking parts of the bell were helpful in understanding its substructure. Structural relationships may be inferred between this cytoplasmic component of the flagellum and the recently described flagellar intramembrane particle rings as well as the structures associated with the basal body in isolated, chemically fixed flagella.The bacterial flagellum is a remarkable locomotory organelle whose assembly and function have been extensively studied (37,46). The flagellum is composed of an external, helical filament connected by what may be a flexible coupling, the hook, to basal structures within and beneath the plasma membrane. The flagellar base harbors the machinery for filament rotation, chemotactic signal reception, and flagellar protein export. Flagellar rotation is energized by transmembrane proton (49) or cation (28, 45) gradients. The structural modules coupling the energy derived from downhill ion transport to force generation must form part of the membrane-associated base.Bacteria migrate by modulation of the directional bias of individual flagellar motors (47). A molecular switch appears to change the direction of rotation, because the rotary motor reverses direction without detectable changes in speed. This response to chemotactic signals is thought to be governed by interactions of small cytoplasmic proteins, CheY and CheZ, with the flagellar base (41,54,63,69). The third function of the flagellar apparatus, assembly of the flagellum, is thought to proceed by routing of the component proteins through the flagellar base into the hollow interior of the flagellum (21, 33, 50).The present understanding of bacterial flagellar structure rests largely on work on the peritrichously flagellated Escherichia coli and Salmonella typhimurium and the monoflagellated Caulobacter crescentus. Detergent solubilization of spheroplasts releases flagellar filaments that terminate in a set of basal rings, L/P and M/S (15). The basal rings have been purified together with the hook to make hook-basal body complexes (2,14,16,35,61,62). However, a number of proteins essential for flagellar function are absent from the hook-basal body complexes. These include MotA and MotB (two transmembrane proteins necessary for rotation) (13,60,67,68) and the switch complex (40, 48, 52, 69). The complete basal structure could also include other flagellar gene products whose function is presently unknown (32).Our effort has centered on the development of rapid-freeze * Corresponding author.procedures for the visualization of the total basal structure in situ and its relati...

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A Caulobacter gene involved in polar morphogenesis

Cited by 14 publications

References 34 publications

Expression of an early gene in the flagellar regulatory hierarchy is sensitive to an interruption in DNA replication

Expression of an early gene in the flagellar regulatory hierarchy is sensitive to an interruption in DNA replication

Polarity in Action: Asymmetric Protein Localization in Bacteria

New structural features of the flagellar base in Salmonella typhimurium revealed by rapid-freeze electron microscopy

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