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Journal of Bacteriology, March 1999, p. 1927-1930, Vol. 181, No. 6
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
The Polar Flagellar Motor of Vibrio
cholerae Is Driven by an Na+ Motive
Force
Seiji
Kojima,1
Koichiro
Yamamoto,2
Ikuro
Kawagishi,1 and
Michio
Homma1,*
Division of Biological Science, Graduate
School of Science, Nagoya University, Chikusa-ku, Nagoya
464-8602,1 and Department of Nutritional
Science, Faculty of Health and Welfare Science, Okayama Prefectural
University, Soja, Okayama 719-1197,2 Japan
Received 27 October 1998/Accepted 12 January 1999
 |
ABSTRACT |
Vibrio cholerae is a highly motile bacterium which
possesses a single polar flagellum as a locomotion organelle.
Motility is thought to be an important factor for the virulence of
V. cholerae. The genome sequencing project of this
organism is in progress, and the genes that are highly homologous to
the essential genes of the Na+-driven polar flagellar motor
of Vibrio alginolyticus were found in the genome database
of V. cholerae. The energy source of its flagellar
motor was investigated. We examined the Na+ dependence and
the sensitivity to the Na+ motor-specific inhibitor of the
motility of the V. cholerae strains and present the
evidence that the polar flagellar motor of V. cholerae
is driven by an Na+ motive force.
| |
TEXT |
Many motile bacteria move by
rotating their flagella, the filamentous organelles that extend from
the cell body. Flagellar rotation is carried out by a reversible rotary
motor (about 20 nm in diameter) embedded in the cytoplasmic membrane at
the base of each flagellar filament. These motors are powered by an
electrochemical gradient of specific ions across the cytoplasmic
membrane and are classified into two types of coupling ions: an
H+-driven motor (in Escherichia coli,
Salmonella typhimurium, and Bacillus spp.) and an
Na+-driven motor (in alkalophilic Bacillus and
marine Vibrio spp.) (6, 19). Thus, the flagellar
motor is a tiny and elaborate molecular machine which converts
electrochemical energy into mechanical work. However, the mechanism of
this energy conversion is not clarified at the molecular level.
The study of the flagellar motor has been extensively done for the
H+-driven motor of E. coli and S. typhimurium, and it has been shown that two integral membrane
proteins, MotA and MotB, are essential for force generation in the
motor (12, 29). They have four and a single transmembrane
segment(s), respectively (10, 38), and form a
proton-conducting channel complex responsible for coupling ion
translocation to force generation in the motor (7, 16, 28,
30). The MotA-MotB channel complex is anchored to the cell wall
by a peptidoglycan binding domain of MotB. Some critical residues
involved in torque generation have recently been identified by
intensive mutational studies (8, 9, 37, 39). In the Na+-driven motor, it was shown that four
integral membrane proteins, PomA, PomB, MotX, and MotY, are essential
for force generation in the polar flagellar motor of the marine
bacterium Vibrio alginolyticus (1, 26). MotX and
MotY have also been identified in Vibrio parahaemolyticus
(23, 24). PomA and PomB have similarities to MotA and MotB,
respectively, and so they might also form an Na+ channel
complex and play an important role in force generation in the motor.
Vibrio cholerae is the bacterium that causes cholera. It has
a pathogenic cycle consisting of a free-swimming phase outside its host
and a sessile virulent phase when it is colonizing the human small
intestine. During the free-swimming phase, the organism is highly
motile by means of a single polar flagellum (14). Motility is thought to contribute to the virulence of
V. cholerae, but the relationship between motility and
virulence is not yet understood (14, 27) and basic studies
of its flagellar motor have not been done. As described above, the
flagellar motor has been intensively investigated in other
Vibrio species, namely V. alginolyticus and
V. parahaemolyticus. They have two distinct types of
flagella, a polar flagellum used for swimming in a liquid medium and
numerous lateral flagella used for swarming on the surface of solid
substrate (5, 20, 22, 32, 33). Polar and lateral flagella
rotate by Na+- and H+-driven flagellar motors,
respectively (2, 20). When grown in a liquid medium, the
organism mainly expresses a single polar flagellum and swims rapidly.
Therefore, the cell shape and motility of these Vibrio are
very similar to those of V. cholerae in liquid. It has
also been shown that the flagellar basal body of V. alginolyticus resembles that of V. cholerae
(4, 13). In addition, from the genome sequencing project of
V. cholerae, the partial sequences of genes homologous
to pomA, pomB, motX, and
motY, essential for the rotation of the Na+
motor, have been found in the database. Gardel and Mekalanos (15) reported that the disruption of the pomB
homolog of V. cholerae results in a flagellated but
nonmotile strain (the authors described pomB as
motB, and the partially deduced amino acid sequence of MotB
showed 84% identity to PomB of V. alginolyticus),
suggesting that the pomB homolog of V. cholerae is also essential for force generation in the motor.
Therefore, we think that the polar flagellar motor of V. cholerae might be driven by an Na+ motive force. In
this study, we examined Na+ dependence and the effects of
specific inhibitors on motility in V. cholerae and
present evidence that the polar flagellar motor is driven by an
Na+ motive force.
V. cholerae O139 strain 1854 is highly
motile.
We examined the swarming abilities of the following
V. cholerae strains: 1854 (O139; Bengal serovar
[18]), E8499 (non-O1 [11]), S7 (O37
[35]), N86 (O1; El Tor biotype [36]),
and 569B (O1; Classical biotype [11, 21]). Fresh
colonies on LB solid agar plates (1% tryptone, 0.5% yeast extract,
0.5% NaCl, 1.25% agar) were inoculated onto LB semisolid plates
(0.3% agar) and incubated for 4 h at 37°C. As shown in Fig.
1, strains E8499, 569B, and 1854 made
swarm rings (the ring of strain 1854 was the largest), but S7 and N86
showed very little swarming ability. When cells were cultured in LB
broth to directly observe motility, strain 1854 demonstrated the best
motility of the strains used, consistent with the results of swarming
ability; most of the cells swam very rapidly and the fraction of cells
that were motile was very large compared with that of the other strains
(data not shown). Some of the other strains were also motile, but the
fraction of motile cells was smaller than that of strain 1854, because
of the aggregation or elongation of the cells (data not shown).
Therefore, we mainly used strain 1854 for motility analysis in this
study.
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FIG. 1.
Swarming abilities of V. cholerae
strains. Fresh single colonies of the indicated V. cholerae strains were inoculated onto an LB semisolid plate (0.3%
agar) and incubated for 4 h at 37°C.
|
|
Effect of ionic strength on the swimming speed of V. cholerae 1854.
A previous study of the 5S rRNA sequence
suggested that V. alginolyticus, which has an
Na+-dependent polar flagellum, is closely related to
V. cholerae (4). Therefore, we compared the
motilities by polar flagella of V. cholerae and
V. alginolyticus. These two Vibrio spp. are usually grown in different salt concentrations. In LB medium, which
contains 0.5% NaCl, commonly used for growing V. cholerae, the V. alginolyticus strain VIO5 (wild
type in polar flagellar motility [26]) could not grow
(data not shown). However, in VPG medium (1% polypeptone,
0.5% glycerol, 0.4% K2HPO4, 3% NaCl), commonly using for growing V. alginolyticus,
V. cholerae 1854 grew comparably to V. alginolyticus VIO5. We compared the effects of ionic strength on
the motility of V. cholerae 1854 cells cultured in
these two media. Strain 1854 cells were grown in both LB and VPG media,
and as a control V. alginolyticus VIO5 cells were
cultured in VPG medium. At late log phase, cells were harvested and
resuspended in TMN medium containing 50 mM Tris-HCl, 5 mM
MgCl2, 5 mM glucose, and various concentrations of salts,
and the motility of the cells was observed. As shown in Table
1, when the ionic strength of TMN medium
was fixed at 300 mM, the motility of LB medium-cultured 1854 cells
deteriorated and this deterioration became more severe as the
concentration of NaCl increased. At 300 mM NaCl, both the motile
fraction and the swimming speed were greatly reduced. LB medium-cultured 1854 cells resuspended in media of lower ionic strength
(100 or 200 mM NaCl) showed a larger motile fraction and a greater
swimming speed. However, the VPG-cultured V. cholerae 1854 and V. alginolyticus VIO5 cells showed nearly the
same motile fractions regardless of ionic strength, and their
swimming speeds increased as the NaCl concentration of the medium was
increased. However, the motile fractions were significantly smaller
than that of LB-cultured 1854 cells at 100 mM NaCl. We note that
VPG-cultured 1854 cells showed very tumbly-biased swimming, and
attractants, such as serine or Casamino Acids, were not effective in
suppressing the directional change of swimming. These results indicate
that V. cholerae 1854 can grow in media of a relatively
wide range of ionic strengths, but the greatest motility of
V. cholerae 1854 cells is achieved with an ionic
strength of 100 mM when the cells are cultured in LB medium containing
0.5% NaCl. Therefore, in the following experiments, the total ionic
concentration of Na+ and K+ was fixed to 100 mM
in TMN medium.
Polar flagellar motor of V. cholerae 1854 is
driven by the sodium motive force.
We next examined the
potential for Na+ as an energy source of the polar
flagellar motor of strain 1854. V. cholerae 1854 and V. alginolyticus VIO5 cells were cultured in LB and VPG
media, respectively, and motility was measured in TMN medium containing various concentrations of NaCl, with a salt concentration of 100 mM
attained by adding KCl. As shown in Fig.
2A, both 1854 and VIO5 cells clearly
showed Na+-dependent motility and 1854 cells swam
significantly faster than VIO5 cells did under all conditions.
LB medium-cultured 1854 cells also showed a similar
Na+-dependent motility in the medium whose ionic strength
was fixed at 100 mM by the addition of choline chloride instead of KCl
(data not shown). We also examined the effect of the Na+
motor-specific inhibitor, phenamil, on the motilities of both strains.
Phenamil is known to inhibit the Na+ motor in a
noncompetitive manner with Na+ in the medium
(3). As shown in Fig. 2B, the motilities of both strains
were also clearly inhibited by phenamil in the presence of 50 mM NaCl,
although the concentration of phenamil required to completely
inhibit the motility of V. cholerae was slightly higher
than that needed for V. alginolyticus. Amiloride, which is the analog of phenamil and which specifically inhibits the Na+ motor in a competitive manner with Na+ in
the medium (31), also inhibited the motilities of both
strains (data not shown). These results suggest that the polar
flagellar motor of V. cholerae 1854 is driven by the
Na+ motive force.
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FIG. 2.
Na+-dependent and phenamil-sensitive
motility of V. cholerae 1854. V. cholerae 1854 and V. alginolyticus VIO5 cells were
cultured in LB or VPG medium, respectively. At late log phase, cells
were harvested and resuspended in TMN medium containing various
concentrations of NaCl (A) or in TMN medium (pH 7.5) containing 50 mM
NaCl, 50 mM KCl, and various concentrations of phenamil (B). In the
experiment shown in panel A, the total concentration of salts in TMN
medium was adjusted to 100 mM by the addition of KCl. The swimming
speeds of the cells were obtained as described in Table 1, footnote
c.
|
|
It is known that
V. alginolyticus has an
Na
+-dependent NADH-quinone reductase (NQR) that
functions as a respiration-coupled
Na
+ pump only in an
alkaline pH range (
34). At a neutral pH, the
Na
+
motive force is secondarily generated by a
Na
+/H
+ antiporter from the H
+
motive force. In this case, the addition of the protonophore
carbonyl
cyanide
m-chlorophenylhydrazone (CCCP) collapses the
H
+ motive force and hence the Na
+ motive force.
At an alkaline pH, CCCP collapses the H
+ motive force but
not the Na
+ motive force, which is generated and maintained
by the Na
+ primary pump. The Na
+ pump can
be specifically inhibited by
2-heptyl-4-hydroxyquinoline-
N-oxide
(HQNO). We
examined the effects of CCCP and HQNO on motility in
neutral or
alkaline conditions in order to confirm the
Na
+-dependent motility of
V. cholerae. As shown in Table
2, the
swimming speeds of both 1854 and VIO5 cells in the medium containing
20 µM CCCP at pH 7.5 were severely reduced. At pH 8.5, both 1854
and
VIO5 cells were still motile in the presence of 20 µM CCCP.
However,
the motility of both strains was completely inhibited
by the addition
of 20 µM HQNO to this medium. These results showed
that
V. cholerae as well as
V. alginolyticus
cells are motile
only in the presence of the Na
+
motive force, and we have demonstrated that the polar flagellar
motor
of
V. cholerae is powered by an Na
+ motive
force. These results also suggest that the respiratory
chain of
V. cholerae contains NQR, similar to that of
V. alginolyticus.
This enzyme in
V. alginolyticus was recently reported to be composed
of six
subunits, NQR1 to NQR6 (
17,
25). Partial sequences
of the
genes homologous to
nqr1 and
nqr2 were also found
in the
genome database of
V. cholerae, consistent with
our physiological
results. Actually,
nqrB (
=nqr2)
was recently identified in
V. cholerae (
16a).
Considering the evolutionarily close relation
between these two
Vibrio spp. revealed by the analysis of 5S rRNA
sequences
(
4), they should have many other similar physiological
characters. Some distinct aspects between them were found in the
present study. For example,
V. cholerae cells swim
faster than
V. alginolyticus cells under certain
conditions. The genome sequence
of
V. cholerae revealed that it has homologous genes coding
for
the essential components of the Na
+ motor, i.e.,
pomA,
pomB,
motX, and
motY,
which are all of the
Na
+ motor genes identified until now.
These two
Vibrio spp. have
very similar polar flagellar
basal body structures (
4). Thus,
subtle differences in
these motor components between these species
might cause differences in
the efficiency of energy conversion
in the Na
+ motor. We
hope that the comparative studies of Na
+ motors in these
two species will reveal some cues for clarifying
the mechanism of
mechanochemical coupling in Na
+-driven flagellar
motors.
| |
ACKNOWLEDGMENTS |
This work was supported in part by grants-in-aid for scientific
research from the Ministry of Education, Science and Culture of Japan
(to I.K. and M.H.) and from the Japan Society for the Promotion of
Science (to S.K.).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Division of
Biological Science, Graduate School of Science, Nagoya University,
Chikusa-ku, Nagoya 464-8602, Japan. Phone: 052-789-2991. Fax:
052-789-3001. E-mail:
g44416a{at}nucc.cc.nagoya-u.ac.jp.
| |
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Journal of Bacteriology, March 1999, p. 1927-1930, Vol. 181, No. 6
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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