Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway

Gegner, Julie A.; Graham, Daniel R.; Roth, Allan C.; Dahlquist, Frederick W.

doi:10.1016/0092-8674(92)90247-a

Cited by 340 publications

(416 citation statements)

References 26 publications

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“…We hypothesize that E. coli filaments sense chemoattractants and chemorepellents via MCPs concentrated to regions at the poles and all along the cell body and that this mechanism allows normal chemotactic responses. In this model, local pools of CheY, present at a concentration of 10 M in the cytoplasm (8), are acted upon by polar and laterally located MCP clusters. CheY-P then diffuses from the MCP cluster to nearby flagella.…”

Section: Discussionmentioning

confidence: 99%

Motility and Chemotaxis of Filamentous Cells of Escherichia coli

Maki¹,

Gestwicki²,

Lake³

et al. 2000

J Bacteriol

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Filamentous cells of Escherichia coli can be produced by treatment with the antibiotic cephalexin, which blocks cell division but allows cell growth. To explore the effect of cell size on chemotactic activity, we studied the motility and chemotaxis of filamentous cells. The filaments, up to 50 times the length of normal E. coli organisms, were motile and had flagella along their entire lengths. Despite their increased size, the motility and chemotaxis of filaments were very similar to those properties of normal-sized cells. Unstimulated filaments of chemotactically normal bacteria ran and stopped repeatedly (while normal-sized bacteria run and tumble repeatedly). Filaments responded to attractants by prolonged running (like normal-sized bacteria) and to repellents by prolonged stopping (unlike normal-sized bacteria, which tumble), until adaptation restored unstimulated behavior (as occurs with normal-sized cells). Chemotaxis mutants that always ran when they were normal sized always ran when they were filament sized, and those mutants that always tumbled when they were normal sized always stopped when they were filament sized. Chemoreceptors in filaments were localized to regions both at the poles and at intervals along the filament. We suggest that the location of the chemoreceptors enables the chemotactic responses observed in filaments. The implications of this work with regard to the cytoplasmic diffusion of chemotaxis components in normal-sized and filamentous E. coli are discussed.Escherichia coli organisms have about six flagella, located randomly around their surfaces, that serve to propel the bacterium. When flagellar rotation is counterclockwise, the flagella form a bundle at one end to push the bacterium forward; this is known as a "run" and typically lasts about 1 to 2 s. When the rotation is clockwise, the flagella pull in opposing directions, causing the bacterium to "tumble" for less than a second. The bacteria alternately run and tumble in the absence of stimuli. When an attractant is encountered, running is promoted and tumbling is suppressed, which causes the bacteria to swim towards the attractant. When a repellent is encountered, the bacteria tumble, which prevents them from swimming into repellent. Adaptation to the attractant or repellent returns the bacteria to unstimulated behavior despite the continued presence of attractant or repellent.Detection of attractants and repellents is mediated by a series of chemoreceptors in the cytoplasmic membrane, the methyl-accepting chemotaxis proteins (MCPs). Binding of repellents induces phosphorylation of the soluble cytoplasmic protein CheY, whereas binding of attractants results in CheY dephosphorylation. CheY interacts with the flagellar motor components and controls the direction of flagellar spin; phosphorylated CheY (CheY-P) stimulates clockwise rotation (tumbling), while unphosphorylated CheY results in counterclockwise rotation (running). For recent reviews of motility and chemotaxis see references 7 and 30.The MCPs are located primarily at t...

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Section: Discussionmentioning

confidence: 99%

Motility and Chemotaxis of Filamentous Cells of Escherichia coli

Maki¹,

Gestwicki²,

Lake³

et al. 2000

J Bacteriol

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“…The inhibition of E. coli chemotaxis was also observed when E. coli cheW was overexpressed in E. coli (Sanders et al, 1989). A stable quaternary structure is thought to form between an MCP ᮊ 1997 Blackwell Science Ltd, Molecular Microbiology, 24, 41-51 dimer, two molecules of CheW and a CheA dimer (Gegner et al, 1992). The change in ligand binding to the receptor is transmitted through the MCP and CheW, resulting in the activation of CheA.…”

Section: Discussionmentioning

confidence: 99%

Characterization of the chemotaxis protein CheW from Rhodobacter sphaeroides and its effect on the behaviour of Escherichia coli

Hamblin

Bourne

Armitage

1997

Molecular Microbiology

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SummaryIn contrast to the situation in enteric bacteria, chemotaxis in Rhodobacter sphaeroides requires transport and partial metabolism of chemoattractants. A chemotaxis operon has been identified containing homologues of the enteric cheA, cheW, cheR genes and two homologues of the cheY gene. However, mutations in these genes have only minor effects on chemotaxis. In enteric species, CheW transmits sensory information from the chemoreceptors to the histidine protein kinase, CheA. Expression of R. sphaeroides cheW in Escherichia coli showed concentrationdependent inhibition of wild-type behaviour, increasing counter-clockwise rotation and thus smooth swimming -a phenotype also seen when E. coli cheW is overexpressed in E. coli. In contrast, overexpression of R. sphaeroides cheW in wild-type R. sphaeroides inhibited motility completely, the equivalent of inducing tumbly motility in E. coli. Expression of R. sphaeroides cheW in an E. coli ⌬cheW chemotaxis mutant complemented this mutation, confirming that CheW is involved in chemosensory signal transduction. However, unlike E. coli ⌬cheW mutants, inframe deletion of R. sphaeroides cheW did not affect either swimming behaviour or chemotaxis to weak organic acids, although the responses to sugars were enhanced. Therefore, although CheW may act as a signal-transduction protein in R. sphaeroides, it may have an unusual role in controlling the rotation of the flagellar motor. Furthermore, the ability of a ⌬cheW mutant to swim normally and show wild-type responses to weak acids supports the existence of additional chemosensory signal-transduction pathways.

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“…In vitro protein-protein interaction experiments indicate that CheW and CheA from E. coli are capable of forming a thermodynamically stable complex with chemoreceptors under physiological conditions (11,35). If R. centenum CheWCheAY forms a stable complex with receptors, communication with the polar flagellar motor would require that receptors be located near flagella.…”

Section: Discussionmentioning

confidence: 99%

Analysis of a chemotaxis operon from Rhodospirillum centenum

Jiang

Bauer

1997

J Bacteriol

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A chemotaxis gene cluster from the photosynthetic bacterium Rhodospirillum centenum has been cloned, sequenced, and analyzed for the control of transcription during swimmer-to-swarm cell differentiation. The first gene of the operon (cheAY) codes for a large 108-kDa polypeptide with an amino-terminal domain that is homologous to CheA and a carboxyl terminus that is homologous to CheY. cheAY is followed by cheW, an additional homolog of cheY, cheB, and cheR. Sequence analysis indicated that all of the che genes are tightly compacted with the same transcriptional polarity, suggesting that they are organized in an operon. Cotranscription of the che genes was confirmed by demonstrating through Western blot analysis that insertion of a polar spectinomycin resistance gene in cheAY results in loss of cheR expression. The promoter for the che operon was mapped by primer extension analysis as well as by the construction of promoter reporter plasmids that include several deletion intervals. This analysis indicated that the R. centenum che operon utilizes two promoters; one exhibits a 70 -like sequence motif, and the other exhibits a 54 -like motif. Expression of the che operon is shown to be relatively constant for swimmer cells which contain a single flagellum and for swarm cells that contain multiple lateral flagella.More than a century ago, Engelmann (7) observed that when purple sulfur photosynthetic bacteria of the genus Chromatium were illuminated with a broad spectrum of light, the cells accumulated at wavelengths that corresponded to the in vivo absorption peaks of the cells. A more accurate description of this phenomenon is that when smooth-swimming cells migrate into a dark region (or into regions of the spectrum where wavelengths are not absorbed by photopigments), they either tumble or reverse the direction of movement, depending on the species. The phenomenon has been termed a scotophobic (fear of darkness) response since the cells exhibit an aversion to darkness rather than a specific affinity for light (12,29). Since a reduction in light intensity causes a tumbling/reversal response, the mechanism of moving through an increasing gradient of light intensity appears to involve a directed "random walk" such that the length of smooth swimming is longer when cells are going up a light gradient than when they are going down. Superficially, this process is not unlike the wellcharacterized bacterial "trial-and-error" walking up a chemical gradient that is mediated by chemoreceptors and the Che protein phosphorylation cascade (2, 40).The mechanism whereby a reduction in light intensity causes a tumbling/reversal response is still unclear. However, recent work has revealed that a functioning photosynthetic apparatus is required for photosensory perception (3). In addition, chemical inhibition of electron carrier components such as the cytochrome bc 1 complex, are incapable of light perception (4). These results have led to the current dogma that the scotophobic response is mediated by the perception of a sudden decre...

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Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway

Cited by 340 publications

References 26 publications

Motility and Chemotaxis of Filamentous Cells of Escherichia coli

Motility and Chemotaxis of Filamentous Cells of Escherichia coli

Characterization of the chemotaxis protein CheW from Rhodobacter sphaeroides and its effect on the behaviour of Escherichia coli

Analysis of a chemotaxis operon from Rhodospirillum centenum

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