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Journal of Bacteriology, February 2003, p . 1190-1194, Vol . 185, No . 4

Effect of Intracellular pH on Rotational Speed of Bacterial Flagellar Motors{dagger}

Tohru Minamino,1 Yasuo Imae,2 Fumio Oosawa,3 Yuji Kobayashi,4 and Kenji Oosawa1,5*

Protonic NanoMachine Project, ERATO, JST, Seika, Kyoto 619-0237,,1 Institute of Molecular Biology, Faculty of Science,2 Graduate School of Mathematics, Nagoya University, Chikusa-ku, Nagoya 464-8602,5 Aichi Institute of Technology, Toyota 470-0392,3 Graduate School of Pharmaceutical Sciences, Osaka University, Suita, Osaka 565-0871, Japan4

Received 6 September 2002/ Accepted 22 November 2002


   ABSTRACT

 
Weak acids such as acetate and benzoate, which partially collapse the transmembrane proton gradient, not only mediate pH taxis but also impair the motility of Escherichia coli and Salmonella at an external pH of 5.5 . In this study, we examined in more detail the effect of weak acids on motility at various external pH values . A change of external pH over the range 5.0 to 7.8 hardly affected the swimming speed of E . coli cells in the absence of 34 mM potassium acetate . In contrast, the cells decreased their swimming speed significantly as external pH was shifted from pH 7.0 to 5.0 in the presence of 34 mM acetate . The total proton motive force of E . coli cells was not changed greatly by the presence of acetate . We measured the rotational rate of tethered E . coli cells as a function of external pH . Rotational speed decreased rapidly as the external pH was decreased, and at pH 5.0, the motor stopped completely . When the external pH was returned to 7.0, the motor restarted rotating at almost its original level, indicating that high intracellular proton (H+) concentration does not irreversibly abolish flagellar motor function . Both the swimming speeds and rotation rates of tethered cells of Salmonella also decreased considerably when the external pH was shifted from pH 7.0 to 5.5 in the presence of 20 mM benzoate . We propose that the increase in the intracellular proton concentration interferes with the release of protons from the torque-generating units, resulting in slowing or stopping of the motors .


   INTRODUCTION

 
The bacterial flagellar motor, which is embedded within the cytoplasmic membrane, is a rotary machine to generate motility (1, 15) . The motor is placed in either of two states, counterclockwise rotation and clockwise rotation, which cause swimming and tumbling, respectively . The switch in the direction of flagellar motor rotation is the basis of chemotaxis . In Escherichia coli and Salmonella, the motor is driven by the transmembrane electrochemical gradient of protons (H+), i.e., the proton motive force (17, 18) . Although many studies have been carried out, it still remains unknown how the motors convert the proton influx into the energy for generating torque .

Based on genetic analyses of mutants with paralyzed phenotypes, five proteins are known to be responsible for torque generation in the flagellar motor: MotA, MotB, FliG, FliM, and FliN . MotA and MotB are cytoplasmic membrane proteins and together form a complex . The MotA/MotB complex is responsible for proton conductance and functions as a torque-generating unit (2, 3) . Since MotB is postulated to be anchored to the peptidoglycan layer, the complex could be the stator (4) . FliG, FliM, and FliN are involved in torque generation and switching of the direction of flagellar motor rotation (7, 29) . They form the C ring, which is directly mounted onto the cytoplasmic side of the flagellar MS ring and therefore seems likely to be the rotor (6, 23) . It has been suggested that electrostatic interactions at the rotor-stator interface are important for torque generation (31) .

The proton motive force, which consists of membrane potential ({Delta}{psi}) and transmembrane proton gradient ({Delta}pH), is easily manipulated by various methods, such as the addition of ionophores and lipophilic weak acids or the application of electric pulses (8, 10, 12, 17, 18, 24) . Weak acids such as acetate and benzoate cross the membrane in neutral form and then dissociate, thereby lowering the intracellular pH so that {Delta}pH is partially collapsed . It has been shown that weak acids not only mediate pH taxis but also impair the motility of E . coli and Salmonella when the external pH is acidic, suggesting that these phenomena could result from the change in cytoplasmic pH (12, 24, 28) . It remains unknown how the decrease in the intracellular pH interferes with the motility of these bacteria, although Khan et al . (10) have shown that the decrease in motor rotation of Streptococcus with the external pH shifted from 7.5 to 6.0 in the presence of weak acid does not result from reduction of the total {Delta}{psi} .

In this study, to clarify the effect of intracellular proton concentration on rotational speeds of individual flagellar motors in E . coli and Salmonella, we measured both the swimming speed of motile cells and rotational rate of tethered cells at various external pH values in the presence or absence of weak acid . We show that motile cells decrease their swimming speed sharply upon a shift from pH 7.0 to 5.0 in the presence of weak acid . We also show that the total proton motive force of the cells does not differ significantly over this pH range, suggesting that it is the increase in intracellular proton concentration that is responsible for abolishing motility .


   MATERIALS AND METHODS

 
Bacteria and media. E . coli strains AW405 (wild type for motility and chemotaxis) and AW569 (tar tsr) and Salmonella sp . strain SJW3076 [{Delta}(cheA-cheZ)] were used in this study . AW569 and SJW3076 produce an intact flagellar apparatus but rotate their motors exclusively counterclockwise (16, 22) . L broth contained 10 g of Bacto Tryptone (Difco), 5 g of yeast extract (Difco), and 5 g of NaCl per liter . T broth contained 10 g of Bacto Tryptone and 5 g of NaCl per liter . M9 medium contained 100 ml of 10x salts (10 g of NH4Cl, 59 g of Na2HPO4, 30 g of KH2PO4, and 5 g of NaCl), 1 ml of 0.1 M CaCl2, 1 ml of 1 M MgSO4, 20 ml of 50% glycerol, and 3 g of Casamino Acids per liter . Motility medium contained 10 mM potassium phosphate, 0.1 mM EDTA, and 10 mM sodium lactate . The pH of motility medium was adjusted to the desired final pH by addition of HCl or KOH . Potassium acetate and potassium benzoate were added to motility medium at final concentrations of 34 and 20 mM, respectively, since it has been reported that they greatly reduce {Delta}pH and strongly mediate pH taxis of E . coli and Salmonella at these concentrations, when external pH is acidic (12, 24, 28) .

Measurement of swimming speed. E . coli AW569 was grown in T broth containing 10 mM sodium lactate at 37°C with shaking, harvested at an optical density at 590 nm of 0.7, and washed three times with motility medium . Then the cells were suspended in motility medium with or without 34 mM potassium acetate, and the pH of the cell suspension was adjusted by either HCl or KOH . Motile cells were observed at ca . 25°C under a high-intensity dark-field microscope and recorded on videotape . The swimming speed of the cells was measured as described before (22) .

Salmonella sp . strain SJW3076 was grown overnight in L broth at 37°C with shaking, washed once with motility medium at pH 7.0, and suspended in motility medium . The cells were then diluted 1:100 into motility medium at the desired pH with or without 20 mM benzoate . They were then placed under a phase-contrast microscope (CH40; Olympus Co., Tokyo, Japan) at room temperature (ca . 22 to 25°C), and their motile behavior was videotaped with a charge-coupled device camera (C5405-50; Hamamatsu Photonics, Hamamatsu, Japan) and a Sony WV-DR7 videorecorder (Sony Co., Tokyo, Japan) . The swimming speeds of the cells were measured by an image-analyzing system (Move-tr/2D; Library Co., Tokyo, Japan) .

Measurement of {Delta}{psi}. The {Delta}{psi} of AW569 cells was measured at ca . 25°C by uptake of a membrane-permeable radioactive cation, [3H]triphenylmethylphosphonium ion ([3H]TPMP), as described by Oosawa and Imae (22) .

Measurement of intracellular pH. The intracellular pH of AW569 cells was measured at ca . 25°C by 31P nuclear magnetic resonance (NMR), as described by Slonczewski et al . (27) . The cells were grown exponentially in M9 medium (the swimming speed of the motile E . coli cells was essentially the same in M9 medium and T broth) . The cells were cooled on ice with mixing and washed once with NMR buffer (100 mM HEPES, 50 mM morpholineethanesulfonic acid [MES], 80 mM NaCl, and 5 mM potassium phosphate, pH 7.4) and finally suspended to a cell concentration of 50% (wt/vol) in the NMR buffer at the desired pH with or without 34 mM acetate . 31P-NMR spectra were obtained at 145.7 MHz on a WM-360 wide-bore spectrometer (Bruker, Rheinstetten, Germany) with vigorous oxygenation maintained throughout .

Tethering procedure. E . coli AW405 and Salmonella sp . strain SJW3076 were grown at 37°C in T broth containing 10 mM sodium lactate and in L broth, respectively, until the cell density reached an optical density at 590 nm of 0.7 . Tethered cells were prepared according to the protocol of Silverman and Simon (26) with minor modifications . The rotation mode of the tethered cells was observed with a dark-field microscope at 25°C and recorded on videotape .


   RESULTS

 
Effect of potassium acetate on swimming speed of E . coli cells. We measured the swimming speed of E . coli AW569 (tar tsr) over an external pH range from 5.0 to 7.8 in the presence or absence of 34 mM potassium acetate (Fig . 1) . The cells swam at ca . 24.5 µm/s in pH 7 motility medium without 34 mM potassium acetate . Over the pH range of 5.0 to 7.8, the average swimming speed varied only slightly, in agreement with previous data (2, 5, 11) . In contrast, in the presence of acetate, the swimming speed did not change much over the pH range of 7.0 to 7.8 but decreased sharply between pH 7.0 and 5.0 . Since the smooth-motile behavior of the E . coli tar tsr double mutant is unchanged before and after acetate addition at pH 5.5 (12, 28), we conclude that it is reduction of the speed of flagellar motor rotation that is responsible for the reduction in swimming speed under these conditions .


FIG . 1 . pH dependency of swimming speed of E . coli AW569 (tar tsr) in the presence ({circ}) and absence (•) of 34 mM potassium acetate . Cells were grown in T broth containing 10 mM sodium lactate . Swimming speed was measured in motility medium at the desired pH.

 
Effect of benzoate on swimming speed of Salmonella cells. To test whether Salmonella flagellar motors are affected similarly to those of E . coli, we measured the swimming speed of Salmonella sp . strain SJW3076 [{Delta}(cheA-cheZ)] at various pH values in the presence or absence of weak acid . An overnight culture of SJW3076 cells was diluted 1:100 in motility medium at the desired pH (7.0, 6.3, or 5.5) with or without 20 mM potassium benzoate, and the swimming speeds of the cells were measured . In the absence of benzoate, the average swimming speeds were ca . 13.7, 15.9, and 16.4 µm/s at external pH values of 7.0, 6.3, and 5.5, respectively . In contrast, the cell speed decreased significantly when the external pH was decreased in the presence of benzoate (ca 12.8, 8.6, and 5.9 µm/s at pH 7.0, 6.3, and 5.5, respectively) . We obtained essentially the same results with 34 mM potassium acetate . The rotational speed of 40-nm fluorescent beads attached to individual filamentless flagellar motors has been shown to be much lower in motility medium containing 20 mM benzoate at pH 6.3 than at pH 7.0 (T . Minamino, unpublished data), further supporting the conclusion that Salmonella flagellar motor function is impaired at low pH in the presence of weak acid .

Effect of acetate on the proton motive force of E . coli cells. The flagellar motors of E . coli and Salmonella are powered by the proton motive force, consisting of {Delta}{psi} and {Delta}pH . Upon the addition of weak acid, the {Delta}pH of the cells is partially collapsed . To examine the effect of weak acid on the total proton motive force of AW569 cells, both {Delta}{psi} and {Delta}pH values were measured, using [3H]TPMP and 31P-NMR, respectively, at various external pH values in the presence or absence of 34 mM potassium acetate (Fig . 2) .


FIG . 2 . pH dependency of {Delta}{psi} (A), {Delta}pH (B), and the total proton motive force (C) of AW569 (tar tsr), in the presence ({circ}) and absence (•) of 34 mM potassium acetate.

 
{Delta}{psi} was not affected by 34 mM acetate (Fig . 2A), while {Delta}pH decreased in the presence of acetate (Fig . 2B), and hence the total proton motive force was weaker in the presence of acetate than in the absence of acetate over the pH range of 5.7 to 6.9 (Fig . 2C) . The swimming speed of E . coli cells measured at pH 5.7 was much lower than that at pH 7.0 when acetate was present (Fig . 1), while the total proton motive force of the cells was essentially the same at pH 5.7 and 7.0 (Fig . 2C) . Although the total proton motive force under the pH 5.7 and 7.0 conditions without acetate was different (124 mV at pH 5.7 and 110 mV at pH 7.0), motility remained constant (Fig . 1) . These results indicate that the total proton motive force is not responsible for the inhibition of motility when intracellular pH is acidic .

Restoration of flagellar motor rotation by decreasing the intracellular proton concentration. To examine whether high intracellular proton concentration irreversibly abolishes flagellar motor function, we observed the dynamics of single flagellar motors through rotational measurements of tethered cells of E . coli and Salmonella as the external pH was changed over the range of 7.0 to 5.0 in the presence of weak acid (Fig . 3) . When the cells at pH 7.0 were abruptly subjected to a lower pH, the rotational rates of the motors declined; the motors of E . coli and Salmonella stopped at pH 5.0 and 5.5, respectively . When the cells were then subjected to an upward pH jump, the stopped motors immediately restarted, and at pH 7.0, the rotational rate was restored to almost its original level, demonstrating that the reduced activity of the motors can be restored by decreasing the intracellular proton concentration .


FIG . 3 . Change in rotation rates of single flagellar motors of E . coli AW405 (wild type) (A) and Salmonella sp . strain SJW3076 [{Delta}(cheA-cheZ)] (B) with external pH shifted in the presence of 34 mM potassium acetate and 20 mM potassium benzoate, respectively . The cells were tethered to a glass slide by a single flagellar filament . The tethered cells at pH 7.0 were abruptly subjected to a lower pH ({circ}) and were later returned to pH 7.0 (•) . For each cell, the rotation rates at the different pH values were normalized to the rate at pH 7.0.

 

   DISCUSSION

 
E . coli and Salmonella flagellar motors are driven by the proton motive force (17, 18) . However, it remains unknown how the motors convert proton influx into torque . In this study, we have examined the effect of intracellular pH on rotational speed of E . coli and Salmonella motors and have shown that their function is severely impaired upon a shift from pH 7.0 to 5.0 in the presence of weak acid (Fig . 1) . At pH 5.7, the motility of E . coli cells was significantly reduced in the presence of weak acid, while the decrease in the total proton motive force of the cells was small (about 14 mV) (Fig . 2), indicating that inactivation of the motors is not a simple matter of reducing the proton motive force . This suggests that the increase in the cytoplasmic proton concentration impairs motility . Furthermore, although tethered cells completely stopped at acidic pH, the rotational rate was restored to almost its original level upon a pH jump from acidic pH back to neutral pH (Fig . 3), indicating that the high intracellular proton concentration does not cause irreversible damage to motor function . Taking the results together, we propose that the absolute concentration of protons in the cytoplasm is one of the factors that determine the rotational rate of the motor .

Yoshida et al . (30) have shown that an increase in intracellular Na+ concentration results in poor motility of Vibrio alginolyticus and have proposed that the torque-generating unit of its Na+-driven motor has an intracellular Na+-binding site, which is distinct from an external one . In this study, we have shown that the rotational speed of the motor did not change so much when only the external proton concentration increased . In contrast, when both the external and intracellular proton concentrations increased, the speed decreased remarkably (Fig . 1) . The thermodynamic driving force, the proton motive force, was not greatly affected at various pHs (Fig . 2) . Since the inhibition of flagellar motor rotation by the decrease in intracellular pH was relieved by increasing the intracellular pH (Fig . 3), we also suggest that the torque generator of the proton-driven motor has an intracellular proton-binding site where cytoplasmic protons kinetically interfere with the motor rotation . When the affinity of intracellular protons for the cytoplasmic proton-binding site is not too low, the protons can saturate this site and so kinetically interfere with proton dissociation to the cytoplasm, resulting in slowing or stopping the motors, as was observed experimentally .

Both protonation and deprotonation of Asp-32 of E . coli MotB, which is located near the cytoplasmic end of its transmembrane segment and seems likely to have a direct role in the conduction of protons (32), have been suggested to drive conformational changes of the cytoplasmic loop of MotA, which interacts with a rotor (13) . In this study, we suggest that the high intracellular proton concentration is unfavorable to the generation of torque, because it saturates the cytoplasmic proton-binding site within the torque generator . Thus, it seems likely that the high intracellular proton concentration prevents Asp-32 of MotB from deprotonation and that hence the motor slows down .

Certain charged-residue substitutions in MotA and FliG individually impair motor function but when present together give fairly normal function, suggesting that electrostatic interactions at the rotor-stator interface appear to be important for torque generation (31) . Therefore, it is also possible that carboxylate groups, which are responsible for the electrostatic interactions, are partially neutralized at low pH, resulting in slowing or stopping of the motor .

Oosawa and colleagues (20, 21) have proposed two cycle models for the energy coupling between motor rotation and the proton influx . One is that the stator having protons interacts with the rotor to generate the torque effectively . The other is that the stator without protons interacts with the rotor to efficiently drive the rotation . In the former model, high pH values inside and outside are unfavorable to the generation of torque, while, in the latter model, low pH values inside and outside are unfavorable . In this study, we have shown that the rotation speed of the motor decreases significantly when both extracellular and intracellular proton concentrations increase, suggesting that the motor may be driven by the latter one .

It has been reported that speedups, slowdowns, and pauses of flagellar motor rotation occasionally occur even during steady rotation intervals (9, 14, 19, 25) . In this study, we have found that rotational rates decreased sharply upon the shift from pH 7.0 to 5.0 in the presence of weak acid (Fig . 1 and 3) . It is possible that the fluctuation of angular velocity of the motor may increase considerably at acidic pH in the presence of weak acid; pauses might also occur more frequently . We are carrying out rotation measurements of single flagellar motors of Salmonella with nanometer spatial resolution and submillisecond temporal resolution at acidic pH in the presence of weak acid to test these hypotheses .

 


   ACKNOWLEDGMENTS

 
We acknowledge Robert M . Macnab for critical reading of the manuscript and helpful comments and Keiichi Namba for continued support and encouragement .


   FOOTNOTES

 
* Corresponding author . Mailing address: Graduate School of Mathematics, Nagoya University, Chikusa-ku, Nagoya 464-8602, Japan . Phone: 81-52-789-2834 . Fax: 81-52-789-2829 . E-mail: kenji{at}math.nagoya-u.ac.jp .

{dagger} This article is dedicated to Yasuo Imae, who died suddenly of a cerebral hemorrhage on 2 July 1993 .


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