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Chapter 11 : Flagellar Switch

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Abstract:

Underlying the flagellum is a large genetic system of more than 40 genes. Many of these are structural, whereas others are responsible for control of gene expression and for assembly of the organelle. In this chapter, the author focuses only on those that are relevant to motor rotation and switching. In fact, only three proteins (FliG, FliM, and FliN) have been found to give rise to defective switching. Mutant searches have been quite extensive, and for the three switch proteins that have been identified, many examples of switch-defective mutations have been found, as described in the chapter. The chapter addresses the extensive studies from which several conclusions can be drawn: suppression is extremely easy to achieve, suppression of a CheY or CheZ mutation by a switch mutation is not allele specific, the three switch proteins differ greatly in the spectrum of mutations generating a given phenotype, positions generating the different phenotypes tend to cluster, and many switch mutations involve charge shifts. Next, the results of this mutant analysis for each of the three proteins are discussed in more detail. Models for the mechanism of switching are intimately related to models for the mechanism for rotation.

Citation: Macnab R. 1995. Flagellar Switch, p 181-199. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch11

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Figures

Image of FIGURE 1
FIGURE 1

Bacterial flagellum and its relationship to various elements of cell surface. This represents the state of knowledge until quite recently, with the approximate location of the motor/switch (dotted outline) inferred but not yet demonstrated experimentally.

Citation: Macnab R. 1995. Flagellar Switch, p 181-199. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch11
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Image of FIGURE 2
FIGURE 2

Flagellar basal body together with associated structures. The cytoplasmic C ring and the extension of the MS ring are seen in electron micrographs of isolated flagella in vitreous ice or negative stain ( ); a related structure has also been seen in freeze-substituted thin sections of cell envelopes ( ). Several lines of evidence indicate that the three motor/switch proteins are present in these structures, with FliG being located directly below the MS ring (which is made out of FliF subunits), and FliM and FliN forming all or part of the C ring. Protein complexes or “studs” seen in freeze-fracture images of whole cells ( ) are believed to consist of the Mot proteins, MotA and MotB, located in the membrane around the circumference of the MS ring and perhaps just above the C ring.

Citation: Macnab R. 1995. Flagellar Switch, p 181-199. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch11
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Image of FIGURE 3
FIGURE 3

Schematic of protein sequences of motor/switch proteins FUG, FliM, and FliN, with sites of mutations giving rise to abnormally high CW bias [Che(CW)], abnormally high CCW bias [Che(CCW)], or paralysis (Mot). Single-site mutations are indicated by flags of open circles, stippled circles, and black triangles, respectively, while in-frame deletions are indicated by bars. FliG and FliM are of essentially the same length, whereas FliN is much shorter. For discussion of the data, see the text. For the actual amino acid changes involved, see and .

Citation: Macnab R. 1995. Flagellar Switch, p 181-199. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch11
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Image of FIGURE 4
FIGURE 4

Model for flagellar motor and switch, based in part on experimental information and in part on speculation (see text). The view is from the cytoplasm, looking along the basal-body axis toward the exterior. The MS ring, located in the cell membrane, consists of about 26 subunits of FliF ( ). At its cytoplasmic face and toward the outer radius of the ring are attached subunits of the motor/switch protein FliG, in a 1:1 stoichiometry with FliF subunits ( ). The other two motor/switch proteins, FliM and FliN, lie at a larger radius than FliG and extend much farther into the cytoplasm, forming the C ring ( ) (cf. Fig. 2 ). FliM is shown here to be more cytoplasm-proximal than FliN, on the premise that it must be available for binding CheY-P, but this is not a strong prediction. FliM and FliN are probably in a 1:1 stoichiometry to each other (Kihara and Macnab, unpublished data); here, they are also shown to be present in the same stoichiometry of 26 subunits as FliF and FliG, but their actual stoichiometry is not known. FliG is part of the rotor, but it is not known whether FliM and FliN are part of the rotor or the stator. The Mot proteins are in the cell membrane surrounding the M ring and behind the C ring. Based on electron microscopy, they are thought to be present in about 12 copies ( ); here, they are arbitrarily shown to be present in 13 copies, and so they are in register with every second FliG-FliM-FliN complex. Depending on the CheY-P concentration (and to a lesser extent the CheY concentration), there will be a time-averaged occupancy of binding sites on FliM, which will determine the probability that the switch will, as a cooperative unit, be in the CCW or CW state (indicated schematically here by the tilt angle of the FliM subunits, although there is no evidence that this is the actual mechanism). It goes back and forth stochastically between the two states at the corresponding probabilities. The arrows indicate the favored state, not the actual switching events (i.e., the figure does not correspond to the switching equilibrium given by the equation in the text).

Citation: Macnab R. 1995. Flagellar Switch, p 181-199. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch11
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Image of FIGURE 5
FIGURE 5

Torsional stress in the motor under different conditions. The tilted lines representing switch state (CCW or CW) are similar to the arrays of half-sites on the rotor of the model of ,so that protons moving in an axial direction from outside to inside along pairs of half-sites Com the rotor and the stator cause an obligatory rotation of the rotor. (A) A motor in the CCW switch state and rotating CCW as a result of the motor torque generated by the inward proton flux experiences a torsional stress resulting from the opposing drag torque from the medium; this stress will tend to destabilize the CCW state, although presumably not enough to cause a switching event to occur. (B) A motor in the CW switch state is being driven in the CCW direction by torque resulting from mechanical and hydrodynamic interactions within a bundle of flagella whose motors are in the CCW switch state. Here, the motor torque is CW (i.e., it constitutes a drag) because protons are being pumped against their gradient. The resulting torsional stress will destabilize the CW switch state and cause the flagellum to go over to the CCW state like the rest of the flagella in the bundle. Although the effects of torsional stress are most easily visualized in the case of the Lauger model, the principle of stress affecting the stability of the switch states applies to other models as well.

Citation: Macnab R. 1995. Flagellar Switch, p 181-199. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch11
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