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Previous Article | Next Article 
J Bacteriol, January 1998, p. 231-235, Vol. 180, No. 2
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Chemotaxis in Borrelia burgdorferi
Wenyuan
Shi,1,2,*
Zhaomin
Yang,1,2
Yongzhi
Geng,1,2
Lawrence E.
Wolinsky,1 and
Michael
A.
Lovett3
School of Dentistry,1
Molecular Biology Institute,2 and
Department of Microbiology and
Immunology,3 University of California, Los
Angeles, Los Angeles, California 90095-1668
Received 14 April 1997/Accepted 31 October 1997
 |
ABSTRACT |
Borrelia burgdorferi is a motile spirochete which has
been identified as the causative microorganism in Lyme disease. The physiological functions which govern the motility of this organism have
not been elucidated. In this study, we found that motility of B. burgdorferi required an environment similar to interstitial fluid
(e.g., pH 7.6 and 0.15 M NaCl). Several methods were used to detect and
measure chemotaxis of B. burgdorferi. A number of chemical
compounds and mixtures were surveyed for the ability to induce positive
and negative chemotaxis of B. burgdorferi. Rabbit serum was
found to be an attractant for B. burgdorferi, while ethanol
and butanol were found to be repellents. Unlike some free-living
spirochetes (e.g., Spirochaeta aurantia), B. burgdorferi did not exhibit any observable chemotaxis to common sugars or amino acids. A method was developed to produce spirochete cells with a self-entangled end. These cells enabled us to study the
rotation of a single flagellar bundle in response to chemoattractants or repellents. The study shows that the frequency and duration for
pausing of flagella are important for chemotaxis of B. burgdorferi.
| |
INTRODUCTION |
Borrelia burgdorferi is a
spirochete which has been shown to be the causative agent for Lyme
disease (22, 25-27). It normally lives in Ixodes
ticks which feed on mice or deer. The bacteria are transmitted to
humans by tick bites. Infection may spread in the skin, causing the
distinctive lesion (erythema migrans). B. burgdorferi then
enters the bloodstream and invades a variety of host tissues. Some
studies indicate that motility of B. burgdorferi may be
important for pathogenesis of this organism (23, 24).
The motility of B. burgdorferi has been well studied
(5, 8, 9, 16, 20). Like many spirochetes, B. burgdorferi has multiple internal periplasmic flagella (axial
filaments) attached at each cell end that overlap in the cell center
(19). Wild-type B. burgdorferi cells swim,
reverse, and flex (16). It is believed that the direction of
rotation of the two flagellar bundles at two cell ends results in
different swim patterns. During smooth swimming, flagellar bundles at
both ends may rotate in opposite directions as viewed from the center
of the cell. A reversal of direction can occur when both flagellar
bundles switch synchronously. A flexing movement can result when the
two flagellar bundles rotate in the same direction (9, 16).
Some motility and chemotaxis genes of B. burgdorferi have
been identified. They exhibit homology with motility and chemotaxis
genes of Escherichia coli and Bacillus subtilis
(12-14). At present, there is scant understanding of
chemotaxis of B. burgdorferi. In this study, we adapted
several known chemotaxis assays to analyze the chemotactic behavior of
B. burgdorferi.
| |
MATERIALS AND METHODS |
Bacterial strain, media, and growth conditions.
The
avirulent B. burgdorferi strain ATCC B31 was used in this
study. The bacteria were grown in BSK II medium (4)
supplemented with 5% young rabbit serum (Pel-Freez Biologicals) at
34°C as described by Foley et al. (10). Log-phase cells
(optical density at 605 nm [OD605] = 0.04 to 0.06) were
used for the experiments. Chemotaxis buffer consists of 0.15 M NaCl, 10 mM NaH2PO4 (pH 7.6), 10
4 M EDTA,
and 10 mg of bovine serum albumin (BSA) per ml. Sometimes methylcellulose was added to a final concentration of 1% to increase the viscosity of the chemotaxis buffer (7).
Spatial chemotaxis assays. (i) Capillary assay.
The
capillary assay for measuring chemotaxis is similar to those described
by Adler (1) and Greenberg and Canale-Parola (17). To assay chemotaxis, a capillary tube containing a
solution of attractant or repellent is inserted into a suspension of
motile B. burgdorferi cells (~108 cells/ml)
resuspended in the chemotaxis buffer. After incubation at 25°C for
2 h, the contents of the capillary tube are transferred to 0.2 ml
of chemotaxis buffer, and bacteria are counted in a Petroff-Hausser
counting chamber. A Petroff-Hausser chamber is used because colony
counting for B. burgdorferi is difficult. To reduce the
inaccuracy, the results are based on averages of triplicates on each of
two separate capillary assays. A capillary tube containing buffer alone
is used for a background control.
(ii) Cuvette assay.
The cuvette assay is a modified
chemotaxis assay based on the method described by Zhulin et al.
(29). A solution of attractant or repellent is mixed with an
equal volume of 2% melted agarose solution and placed into the bottom
of the cuvette chamber (about 4-mm thickness). After the agarose has
solidified, chemotaxis buffer containing bacterial suspension is
carefully layered on top of the agar. Black paper is used to direct the
light beam through the cuvette 3 mm above the surface of the solidified
agarose. The OD605, measured with a Milton Roy Co. model
Spectronic 21D spectrophotometer, changes over time due to the positive
or negative chemotaxis to chemicals in the bottom agarose. Agarose with
buffer alone was used as a control.
(iii) Plug assay.
The plug assay is very similar to the one
described by Tso and Adler (28). A plug of hard agarose
(1.5%), about 5 mm in diameter, containing the chemical to be tested
is placed in the center of a petri dish. Bacteria grown in BSK II
medium are harvested by low-speed centrifugation (3,000 rpm) and
resuspended with the chemotaxis buffer in a smaller volume that gives
visible turbidity (OD605 = 0.2, ~108
cells/ml). Then the bacterial solution is mixed with an equal volume of
0.4% agarose in chemotaxis buffer (prewarmed at 45°C) and poured
into the petri dish. A clear zone around the hard agar plug can be
observed in 2 h if the plug contains repellents.
Temporal chemotaxis assay.
Using the methods described by
Greenberg and Canale-Parola (17) and Goldstein et al.
(16), we studied cellular behavior of B. burgdorferi via videomicroscopy. Motility is observed with a Zeiss
phase-contrast microscope (Axiophot) with a 40× objective. The
microscopic images are captured by a Zeiss videocamera (ZVS-47DEC) and
recorded by a videocassette recorder (VCR; Panasonic AG-6040) to
examine bacterial motility.
Analyzing the gyration of cells with a self-entangled end.
Cells with a self-entangled end were produced by resuspending cells in
chemotaxis buffer at pH 9.0. These cells only have one active flagellar
bundle at the nontangled end. When the free end rotates CCW
(counterclockwise) (as viewed from the entangled end), it produces a
short-wavelength helical cylinder and pulls the cell forward. When the
free end rotates CW (clockwise), it produces a long-wavelength helical
wave and pushes the cell backward.
| |
RESULTS |
Motility of B. burgdorferi.
Under the microscope, we
observed that B. burgdorferi cells grown in BSK II medium
(with 5% rabbit serum) between 20 and 37°C exhibited motility. When
the growth temperature was >37°C, both the rate of growth and
motility were reduced. B. burgdorferi cells grown at 37°C
were actively motile from early log phase (OD605 < 0.01, ~106 cells/ml) to late log phase (OD605 = 0.08 to 0.1). As the cells grew into stationary phase
(OD605 > 0.1), a marked reduction in motility was
observed.
Under a microscope, B. burgdorferi cells moved at speeds of
2 to 10 µm/s in the growth medium. As reported by Goldstein et al.
(16), unstimulated B. burgdorferi cells swam
forward or backward, paused, and flexed.
One interesting question is whether B. burgdorferi prefers
the use of one particular cell end to swim forward. To answer this question, we used videomicroscopy to follow 20 bacteria cells for a
total of 2 h and found that all of them spent about equal amounts
of time swimming forward by using either end (Table
1). These data indicate no difference in
motility for the two cell ends of B. burgdorferi.
Chemotaxis assays require a defined buffer which allows bacterial
motility. One widely used chemotaxis buffer is phosphate buffer (pH
7.0; 102 M) containing potassium EDTA (104
M). This buffer has been successfully used for chemotaxis studies of
E. coli and Spirochaeta aurantia (1,
17). However, in the present study this buffer did not support
motility for B. burgdorferi. We formulated an alternative
buffer which contained 0.15 M NaCl, 10 mM
NaH2PO4 buffer (pH 7.6), 104 M
EDTA, and 10 mg of BSA per ml. B. burgdorferi cells were
observed to be motile in this buffer for many hours. It is interesting that 0.15 M NaCl and pH 7.6 mimic the conditions for interstitial fluid
in the human body (18), a natural environment for B. burgdorferi. A high concentration of NaCl is needed to make
B. burgdorferi motile in the chemotaxis buffer. We varied
the concentration of NaCl in the buffer and found that 0.1 M NaCl was
minimally required for motility whereas 0.15 M NaCl resulted in the
greatest motility. When 0.15 M NaCl was replaced with 0.15 M KCl, 0.15 M LiCl, 0.1 M MgCl2, or 0.1 M CaCl2, motility
was greatly diminished, suggesting that factors other than the ionic
strength or osmolarity of 0.15 M NaCl modulate the motility of B. burgdorferi. The optimal pH for B. burgdorferi is 7.6, although B. burgdorferi cells exhibit some motility in
solutions with pHs ranging from 4.0 to 9.0. Heavy metal ions such as
Ni2+, Co2+, and Cu2+ were very
toxic to B. burgdorferi motility (data not shown); therefore, EDTA (104 M) was added to chelate these heavy
metal ions. The addition of BSA, a major protein in serum, was found to
help B. burgdorferi cells retain motility for a longer time.
It has been reported that addition of 1% methylcellulose to medium
facilitates spirochetal motility (9, 16). We found that
B. burgdorferi cells were very motile in chemotaxis buffer
with addition of 1% methylcellulose; however, the removal of 1%
methylcellulose had no observable effect on motility. Therefore, most
of the experiments described below were done in chemotaxis buffer
without methylcellulose.
Motility of bacteria can be driven either by proton motive force or by
sodium motive force (3, 15). Since a high concentration of
NaCl was required for motility of B. burgdorferi, we tested whether a sodium-driven flagellar motor played a role in motility of
B. burgdorferi. Proton motive force inhibitors such as
2,4-dinitrophenol (1 mM) and dicyclohexylcarbodiimide (1 mM)
strongly inhibited motility, while 1 mM amiloride, a known
inhibitor of sodium motive force, had no effect on motility. These data
suggest that the flagellar motor of B. burgdorferi may
be driven by the proton motive force.
Chemotaxis of B. burgdorferi.
Selected spatial
chemotaxis assays consisting of a capillary assay, a cuvette assay, and
a plug assay (see Materials and Methods) were used to survey the
chemotactic properties of a number of chemical compounds and mixtures.
The capillary assay is a very sensitive assay which enables the
detection of chemoattraction. Usually after 2 h, there are 70 to
200 bacteria in a capillary containing chemotaxis buffer alone, while
there are more than 1,000 cells in the capillary containing
chemoattractants. Chemicals which attract five or more times the
bacteria as the control are considered attractants. The cuvette assay
is a very simple and effective way to study chemotaxis of B. burgdorferi. Unfortunately, it is not very sensitive; the biggest
change in OD605 recorded was about threefold (in response
to undiluted serum). Furthermore, cell precipitation and cell lysis may
also affect the results. The plug assay works particularly well for
negative chemotaxis: repellents in the hard agar plug repel bacteria,
creating a clear zone around the plug.
Table 2 lists the chemicals tested. BSK
II medium (with 5% rabbit serum) was found to be an attractant for
B. burgdorferi. Further analyzing the components of BSK II
medium, we found that the major chemoattraction resulted from the
rabbit serum (Table 2). Serum diluted 200-fold (0.5%) still showed
chemoattraction (Table 2), indicating that the attractant(s) in the
serum must be able to act at a very low concentration. Some of the
known components of serum, such as Fe2+ and hemin, were
tested and found not to be attractants (data not shown). Sugars have
been found to be good attractants for many other bacteria such as
E. coli and S. aurantia (2, 17). A
number of sugars (glucose, lactose, maltose, galactose, and sucrose)
were tested and found not to induce chemotaxis of B. burgdorferi (Table 2). Many amino acids such as serine and
aspartate are excellent attractants for bacteria such as E. coli (21). In this study, single amino acids as well as
complex mixtures like peptone and yeast extract were also tested, and
none were found to attract B. burgdorferi (Table 2).
The plug assays showed that B. burgdorferi moved away from
certain chemicals (negative chemotaxis). Ethanol and other small alcohols were found to be excellent repellents (Table 2). Plugs with
pHs less than 6.5 or higher than 8.5 repelled bacteria (Table 2).
H2O2 and high concentrations of KCl were also
found to have a repellent effect on B. burgdorferi (Table
2). None of these chemicals lysed B. burgdorferi cells at
the concentrations tested (data not shown); therefore, the clear zones
around the plugs were most likely due to negative chemotaxis.
Cellular response to chemicals and adaptation.
Videomicroscopy
was used to study the cellular behavior in response to chemoattractants
and repellents. Unstimulated cells swim forward and backward, flex, and
pause. Usually a bacterium moving fast (>5 µm/s) swims longer (5 to
9 s) and then pauses and flexes less (1 to 2 s); a bacterium
moving slowly (<5 µm/s) swims for a shorter period (3 to 5 s)
and spends more time (2 to 4 s) pausing and flexing. Unstimulated
bacteria usually spent 80 to 85% of the time for smooth swimming and
15 to 20% of the time for flexing and pausing (Fig.
1). After a chemoattractant (e.g., 1%
rabbit serum) was added, the bacteria became almost exclusively smooth
swimming, with rare reversing, pausing, or flexing (Fig. 1a). After a
repellent (e.g., 100 mM ethanol) was added, the bacteria spent most of
time flexing and pausing, with very little time spent smooth swimming
(Fig. 1b). In both cases, after a certain period of time (depending on
the strength of the stimulus), the bacteria adapted to the stimuli and
gradually returned to the regular time ratio for swimming and
flexing-pausing, a behavior called adaptation (Fig. 1).
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FIG. 1.
Cellular behavioral change in response to a
chemoattractant (1% young rabbit serum; a) and a chemorepellent (100 mM ethanol; b). Wild-type B31 cells were used; the testing chemical was
added to bacterial suspension at s 120, as indicated by an arrowhead.
The behavioral change in response to the chemicals was studied by
videomicroscopy, recorded by a VCR, and analyzed frame by frame for the
ratio of time spent swimming and pausing-flexing
(tsw/tp&f). Each data point represents a time
ratio in a 30-s window. Data shown represent the behavioral change of
one representative cell; more than 20 cells were studied, and similar
results were observed.
|
|
Chemotactic behavior of cells with a self-entangled end.
B.
burgdorferi has one flagellar bundle at each cell end; the two
bundles overlap in the cell center. The observed behavior of swimming,
flexing, and pausing is the combined movement of both flagellar
bundles. To understand how the cellular behavior is affected by
rotation of flagella, it is important to study the behavior of a single
flagellar bundle in response to chemoattractants or repellents. To this
end, we used a newly developed method to produce spirochetes which
contain only one active flagellar bundle.
When B. burgdorferi was placed in a solution with a pH of
>8.5, the cell surface seemed to become very sticky. When cells were
resuspended at high density, many of them adhered to form large cell
clumps (Fig. 2a). Cells in the clumps were still alive and motile. When
cells were resuspended at low density, the ends of a small portion
(~1 to 5%) of them became self-entangled. Cells with both ends
self-entangled were found to be nonmotile (data not shown), indicating
that tangling of cell ends with the cell body prevents normal
functioning of the flagellar bundle. Cells with one self-entangled end
were studied (Fig. 2b). These cells have
only one active flagellar bundle located at the nontangled end; the
gyration of this free end indicates the direction of rotation of the
single flagellar bundle. When the nontangled end rotates CCW (as viewed
from the entangled end), it produces a short-wavelength helical
cylinder and pulls the cell forward. When the free end rotates CW, it
produces a long-wavelength helical wave and pushes the cell backward.
We studied the chemotactic behavior of these cells. Without any
stimulus, the free end rotated CCW (pulling cells forward) or CW
(pushing cells backward) or stopped rotation (pausing). With addition
of an attractant (e.g., 1% rabbit serum), the free end rotated
exclusively CCW or CW with almost no pausing (Fig.
3a). When a repellent (e.g., 100 mM
ethanol) was added, the free end was found to have much increased
frequency of pausing, and the duration of each period of pausing was
much longer than for unstimulated cells (Fig. 3b).
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FIG. 2.
Cellular aggregation and self-entanglement of B. burgdorferi. (a) Wild-type B31 cells were grown in BSK II medium
and resuspended at high cell density (OD605 = 0.1) in
solution containing 10 mM NaH2PO4 (pH 9.0),
104 M EDTA, 0.15 M NaCl, and 10 mg of BSA per ml. The
arrowhead indicates a large cell clump. (b) Wild-type B31 cells were
resuspended at low cell density (OD605 = 0.005) in the
buffer described above. The arrowhead indicates a cell with a
self-entangled end.
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FIG. 3.
Gyration of the nontangled cell end in response to a
chemoattractant (1% young rabbit serum; a) and a chemorepellent (100 mM ethanol; b). Low-density bacteria were suspended in solution
containing 10 mM NaH2PO4 (pH 9.0), 0.15 M NaCl,
104 M EDTA, and 10 mg of BSA per ml. After production of
cells with a self-entangled end, the bacteria were resuspended in the
same buffer at pH 7.6 and mixed with testing chemicals at s 60, as
indicated by an arrowhead. The gyration of the nontangled end was
studied by videomicroscopy, recorded by a VCR, and analyzed frame by
frame for the time spent on pushing (indicating CW rotation), pulling
(indicating CCW rotation), and pausing (indicating no rotation). Data
shown represents the behavioral change of one representative cell; more
than 20 cells were studied, and similar results were observed.
|
|
| |
DISCUSSION |
Unique cellular anatomy and distinctive motility enable
spirochetes to move effectively in highly viscous bodily fluids.
Therefore, it is likely that motility and chemotaxis of spirochetes
play a role in pathogenesis. In this work, we studied the chemotactic behavior of B. burgdorferi, a known motile pathogenic
spirochete. We found that B. burgdorferi did not exhibit
chemotaxis toward sugars or amino acids. Instead, it moved toward
serum, which could enable B. burgdorferi to move toward the
bloodstream from tissues. B. burgdorferi avoided high
concentrations of KCl, which could serve as a mechanism for B. burgdorferi to stay in the interstitial fluids (since there is a
high concentration of KCl inside cells) and penetrate through the
cellular junctions. B. burgdorferi tried to avoid hydrogen
peroxide, a chemical released by neutrophils and macrophages to kill
bacteria. This could serve as a protective mechanism for B. burgdorferi in its interaction with the immune system. It is also
interesting that motility of B. burgdorferi requires a high
concentration of NaCl and pH 7.6, which are the normal physiological
conditions for interstitial fluids. In any case, our data suggest that
chemotaxis may indeed be important for the pathogenesis of B. burgdorferi. What we report here is a classic example of
chemotaxis very similar to those studied in other bacteria; however,
through understanding the conditions for motility and chemotaxis of
B. burgdorferi and the chemical nature of attractants and
repellents, we learned a lot about how nature has modified similar
systems for different purposes. In this case, the bacterium is one
which is fully motile inside the human body and may use its chemotaxis
mechanism to find target tissues.
Despite many similarities, there are some fundamental differences
between the chemotaxis of E. coli and that of B. burgdorferi, which holds considerable fascination for those
interested in questions regarding the motility and chemotaxis of
bacteria. One of these questions is how chemotaxis is achieved at the
cellular level. In the case of E. coli, chemotaxis is
achieved by regulating the direction of rotation of the flagellar
bundle. In response to attractants, E. coli flagella rotate
CCW, which forms a bundle at the posterior end and pushes cells
swimming ahead; in response to repellents, E. coli flagella
rotate CW, which makes the bundle fall apart and bacteria tumble.
Therefore, chemotaxis of E. coli is achieved by switching
the direction of rotation of the flagellar bundles. However, for
B. burgdorferi and other spirochetes, in order to swim
forward or backward, the flagellar bundles at two ends of the cell have
to rotate in different directions (6, 9); therefore, simply
switching the rotation direction of flagellar bundles as in E. coli will not produce a similar effect. Instead, coordination of
the two flagellar bundles seems to be important for achieving
chemotaxis at the cellular level (11). The data presented on
chemotaxis of B. burgdorferi are consistent with those of
previous studies of chemotaxis in other spirochetes (11). In
addition, the studies of B. burgdorferi cells with a
self-entangled end suggested that the frequency and duration of pausing
of the flagella are also important in the chemotactic response. In
response to attractants, both of the flagellar bundles of a spirochete rotate without pausing, which could make them coordinate and swim in
one direction. In response to repellents, the flagellar bundles pause
frequently and extensively. This would disrupt the coordination between
two flagellar bundles and cause cells to flex and pause, preventing
cells from going into the repellent area.
| |
ACKNOWLEDGMENTS |
We thank N. W. Charon, S. Goldstein, H. Berg, P. E. Greenberg, N. H. Park, Jon T. Skare, and J. N. Miller for
helpful discussions. We are grateful for the technical assistance of
Steven Ruzin and Hans Holtan at the NSF Center of Plant Developmental
Biology, University of California, Berkeley.
This work was supported by NIH grants GM54666 to W. Shi and AI-29733 to
M. A. Lovett and training grant 5-T32-AI-07323 to Z. Yang.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: UCLA School of
Dentistry and Molecular Biology Institute, P.O. Box 951668, University of California, Los Angeles, Los Angeles, CA 90095-1668. Phone: (310)
825-8356. Fax: (310) 206-5539. E-mail: wenyuan{at}ucla.edu.
| |
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J Bacteriol, January 1998, p. 231-235, Vol. 180, No. 2
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Copyright © 1998, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
