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Journal of Bacteriology, January 2001, p. 763-767, Vol. 183, No. 2
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.2.763-767.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Pseudomonas aeruginosa Exhibits Directed
Twitching Motility Up Phosphatidylethanolamine Gradients
Daniel B.
Kearns,1
Jayne
Robinson,2 and
Lawrence J.
Shimkets1,*
Department of Microbiology, University of
Georgia, Athens, Georgia 30602,1 and
Department of Biology, University of Dayton, Dayton, Ohio
45496-23202
Received 17 July 2000/Accepted 16 October 2000
 |
ABSTRACT |
Pseudomonas aeruginosa translocates over solid surfaces
by a type IV pilus-dependent form of multicellular motility known as
twitching. We wondered whether cells utilize endogenous factors to
organize twitching, and we purified from wild-type cells a lipid that
caused directed movement. Wild-type P. aeruginosa, but not
a pilJ pilus-deficient mutant, showed biased movement up
gradients of phosphatidylethanolamine (PE) established in agar. Activity was related to the fatty acid composition of the lipid, as two
synthetic PE species, dilauroyl and dioleoyl PE, were capable of
directing P. aeruginosa motility while many other species
were inactive. P. aeruginosa PE did not contain either
laurate or oleate, implying that the native attractant species contains
different fatty acids. Uniform concentrations of PE increased cell
velocity, suggesting that chemokinesis may be at least partly
responsible for directed movement. We speculate that PE-directed
twitching motility may be involved in biofilm formation and pathogenesis.
| |
TEXT |
Pseudomonas aeruginosa is
a prevalent contaminant of ventilators and catheters, a common cause of
nosocomial infections, and an opportunistic pathogen: lung infections
with this organism are a leading cause of mortality in both cystic
fibrosis and AIDS patients (27). The aggressiveness and
persistence of this organism may be attributed to the formation of
biofilm microcolonies which protect the component individuals and
concentrate virulence factors (19). Recent studies have
indicated that P. aeruginosa biofilm formation requires
intercellular signaling, and coordinated motility has been implicated
in the proper organization of three-dimensional, mushroom-shaped
structures within the biofilm (7, 9, 22).
P. aeruginosa swims rapidly in liquid by means of flagella,
and during biofilm formation swimming motility is involved in initial
location and adherence to solid surfaces (22). Once attached to a surface, P. aeruginosa moves by the
flagellum-independent surface motility known as twitching
(6). Twitching cells move linearly along their long axis
and are motile only in large groups (24). Twitching may be
powered by retraction of type IV pili (20), and mutants
defective in pilus biosynthesis genes lack twitching motility
(21). Interestingly, mutations resulting in the loss of
pili have also been identified in genes encoding homologs of the
enteric Che chemotaxis proteins (8). In Escherichia coli, these proteins are essential for oriented movement within chemical gradients, suggesting that twitching motility may be chemically regulated. Twitching is absolutely essential for biofilm formation (22).
While directed movement in any surface motile organism is poorly
understood, a chemoattractant has been discovered in the gliding
bacterium Myxococcus xanthus (18). M. xanthus, a nonpathogenic soil bacterium, also forms a biofilm that
requires both cell-cell signaling and surface motility
(25). Gliding motility shares many features with twitching
motility: movement is along the long axis of the cell, occurs in cell
groups, and is dependent on the presence of type IV pili
(16). M. xanthus cells migrate up gradients of
phosphatidylethanolamine (PE) purified from their own cell membranes,
and cells may secrete or otherwise present this chemical to neighboring
cells in order to orchestrate group movement (18). The
extensive similarities between P. aeruginosa and M. xanthus surface motility prompted us to search for an endogenous
lipid produced by P. aeruginosa that functioned as a
twitching chemoeffector.
Twitching motility.
In order to demonstrate twitching
motility, P. aeruginosa PAO1 was grown to late log phase in
L broth (10 g of tryptone, 5 g of yeast extract, and 5 g of
NaCl per liter) and resuspended to 5 × 109 cells/ml
in India ink-MOPS buffer {10 mM
3-(N-morpholino)propanesulfonic acid [pH 7.6], 8 mM
MgSO4, 10% India ink}. One microliter of the cell
suspension was spotted onto TPM agar (10 mM Tris HCl [pH 7.6], 8 mM
MgSO4, 1 mM
KHPO4-KH2PO4 buffer [pH 7.6],
1.5% Bacto agar) and incubated at 37°C for 24 h. The India ink
absorbed to the agar surface and served as a reference point for the
original inoculum. After 24 h, a halo of cells with a rough edge
formed around the origin of the colony, suggesting that P. aeruginosa was capable of twitching at a surface-air interface
(Fig. 1a). Zones of motility were
measured using a Leitz light microscope at a magnification of ×100
with an ocular micrometer. Under these conditions, expansion of
unstimulated swarms occurred at a rate of 31 µm/h.
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FIG. 1.
P. aeruginosa biased twitching motility up PE
gradients. Wild-type PAO1 P. aeruginosa (a and b) and a
pilJ mutant (c and d) were spotted within mock gradients
generated with chloroform (a and c) or PE gradients generated with 10 µg of PE purified from PAO1 in chloroform (b and d). Scale bar = 1 mm.
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A
pilJ mutant was examined to determine whether twitching
motility was responsible for the observed swarm expansion. A
pilJ mutant was constructed by gene replacement with a
tetracycline
resistance (Tc
r) cassette; it completely lacks
twitching motility and expresses
no type IV pili, as determined by
antipilin Western blotting.
The mutation is nonpolar, as the
pilJ locus expressed in
trans restored twitching
motility to the
pilJ mutant (
8). PilJ is
homologous to the
E. coli Tsr chemoreceptor methyl-accepting
chemotaxis
protein, and it is not clear why a mutation in this gene
causes
a twitching motility defect in
P. aeruginosa
(
8). Nonetheless,
the
pilJ mutant produced a
much smaller halo with a smooth edge,
suggesting that the majority of
the zone we observed in wild-type
cells was due to twitching motility
(Fig.
1c).
Purification and identification of twitching chemoeffectors.
A
hydrophobic extract of P. aeruginosa PAO1 was prepared
according to the guidelines of Bligh and Dyer to determine whether P. aeruginosa makes chemicals that effect twitching motility
(4). A volume of 3.75 ml of methanol-chloroform (2:1) was
added to 0.4 g of cells (wet weight) of late-log-phase P. aeruginosa PAO1 and was vortexed for 1 h. The suspension was
centrifuged at 10,000 × g for 5 min and the
supernatant was saved. The pellet was then reextracted with 4.75 ml of
methanol-chloroform-water (2:1:0.8) and centrifuged again, and the
supernatants were combined. Volumes of 2.5 ml of chloroform and 2.5 ml
of water were added to the combined supernatants, vortexed, and
centrifuged to separate the chloroform and aqueous layers. The
chloroform layer containing hydrophobic material was collected and
dried under nitrogen in a preweighed tube. The mass of the residue was
determined and the residue was resuspended in chloroform.
The hydrophobic extract was used to create gradients in agar. A total
of 100 µg of the extract was dried onto a 3-mm diameter
Whatman no. 1 filter paper disk and placed on TPM agar. A disk
with solvent alone
served as a negative control. The plate was
incubated at 32°C for
24 h to generate a gradient, after which
P. aeruginosa
cells, prepared as for the motility assay, were
spotted 3 to 5 mm from
the disk. Colonies spotted near the control
disk produced uniform
halos, but colonies near the disk containing
extract migrated a
distance twofold farther toward the disk than
away from it (data not
shown). The preferential motility suggested
that
P. aeruginosa contained an endogenous, hydrophobic twitching
chemoeffector.
To identify the active molecules, the extract was fractionated by
silica gel affinity chromatography (
12). A total of 20
mg
of extract in hexane-
methyl tert-butyl ether (200:3) was
loaded
on a 2-g column of silica gel (Supelco) that had been washed
with
hexane. The column was then serially eluted with 12 ml of each
solvent listed in Table
1. Each fraction
was dried under nitrogen,
weighed, and resuspended in chloroform. Cells
migrated four- and
threefold farther up gradients generated when 20 µg each of fractions
5 and 6, respectively, was spotted directly on
the agar surface
(Table
1). No biased motility was observed with any
other fraction,
regardless of concentration.
Fraction 5 (100 µg) was resolved by Silica Gel G thin-layer
chromatography (TLC) in chloroform-methanol-water (65:25:4)
until
the solvent was 1 cm from the top of the 20-cm gel. After
resolution,
the plate was stained with iodine vapor, a nonspecific
indicator
of lipids, and with 0.5% ninhydrin (in 1-butanol and 3%
acetic
acid incubated at 100°C for 5 min), a color indicator of free
amino groups (
15). Fraction 5 contained only one
iodine-reactive
band, which had an
Rf value of
0.53, was reactive with ninhydrin,
and comigrated with a PE standard.
The band was verified as PE
by using chloroform-acetone-methanol-acetic
acid-water (10:4:2:2:1)
as an alternative solvent system. Sections of
the plate were scraped,
eluted with methanol, dried under nitrogen, and
resuspended to
a concentration of 1 mg/ml in chloroform. Each eluate
(10 µl)
was spotted directly on a TPM plate and incubated at 32°C
for
24 h to generate a gradient. The fraction containing PE caused
PAO1 to twitch threefold farther up the gradient than down the
gradient
(Fig.
1b). Other fractions displayed no
activity.
While we focused most of our attention on fraction 5, fraction 6 also
contained activity (Table
1) and was resolved with
chloroform-methanol-water (65:25:4) by silica gel TLC. TLC analysis
revealed four iodine-reactive bands. The most intense band was
identified as PE because it had an
Rf value of
0.5, reacted with
ninhydrin, and comigrated with a PE standard. A
second band was
positively stained by ninhydrin and was identified as
phosphatidylserine
based on its
Rf value of 0.15 (
15). A third band did not react
with ninhydrin and was
identified as phosphatidylcholine (PC)
because it had an
Rf value of 0.20 and comigrated with a PC
standard.
The final band had an
Rf value of 1.00 and stained weakly with
ninhydrin. This band has not been identified.
These observations
were confirmed in an alternate solvent system,
chloroform-acetone-methanol-acetic
acid-water (10:4:2:2:1). The
majority of fraction 6 was composed
of PE, which likely accounted for
the activity observed. However,
the other bands were not isolated or
tested
directly.
Mechanism of PE-directed movement.
The pilJ mutant
showed no preferential migration in the presence of purified PE (Fig.
1d). As the pilJ mutant is fully proficient in
flagellum-mediated swimming motility, we concluded that directed movement to PE on surfaces requires twitching motility
(8). We considered two possible explanations for the
PE-dependent directed movement. Either PE could act as a lubricant to
passively facilitate twitching motility, or PE could be a transduced
stimulus mediated by a dedicated perception system to regulate motor
output. The simplest way to address both possibilities was to determine
the specificity of the PE response. One might expect that the
surfactant properties of PE might be less dependent on the fatty acid
side chains than is expected for a transduced stimulus. Six chemically synthesized PE species with different fatty acid side chains were tested to determine the specificity of the motility response. Only dilauroyl (di-C12:0) and dioleoyl
(di-C18:1
9c) PE induced directed motility, suggesting a
significant degree of chemical specificity (Fig.
2). Because PE purified from P. aeruginosa likely contained a wide variety of chemical species,
fatty acid analysis was conducted on PE purified from PAO1 (Microbial
ID, Inc.) (Table 2). The two active
synthetic chemicals cannot account for the activity of the extract,
because the extract lacked both laurate and oleate under the growth
conditions used here. Nonetheless, the specificity of the response
argues against a passive mechanism for PE and favors the involvement of
signal transduction.
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FIG. 2.
P. aeruginosa biased twitching motility up
synthetic dilauroyl and dioleoyl PE. Ten micrograms of each compound
was tested. The preferential migration value is the distance migrated
up the gradient divided by the distance migrated down the gradient. No
preferential movement up the gradient produced a value of 1. Error bars
show the standard deviations of 12 measurements.
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|
Twitching PAO1 individuals have the capacity to reverse direction
within a group of cells, and directed movement may occur
by chemotaxis
(
24). During chemotaxis, an effector excites a
sensory
system to suppress direction reversals and results in
longer periods of
movement toward an attractant (
1). Preferential
movement
continues as long as the concentration continues to increase,
because
an adaptive response continually desensitizes the sensory
system
(
5,
11). Alternatively, PE may increase the speed
of
twitching motility, and therefore directed movement may be
the product
of chemokinesis. Unlike chemotaxis, chemokinesis in
Rhodobacter sphaeroides (
23) and
M. xanthus (
28) does not
show adaptation, and thus the
effect on motility is independent
of a gradient. To distinguish between
chemotactic and chemokinetic
responses in
P. aeruginosa,
cells were spotted onto a uniform
concentration of PE. A total of 0.01, 0.1, or 1 µg of each of
the six chemically synthesized PEs was
delivered to TPM in 10
µl of chloroform and was incubated for 24 h at 32°C. Cells were
then inoculated in the middle of the PE spot
and incubated for
24 h at 32°C, and the swarm expansion rate was
measured with a
30× dissecting microscope and an ocular micrometer. In
the absence
of a gradient, dilauroyl and dioleoyl PE enhanced twitching
motility
approximately threefold (Fig.
3). Unlike the gradient, uniform
concentrations of dimyristoyl PE also enhanced swarm expansion.
Nonetheless, dipalmitoyl, diheptadecanoyl, and distearoyl PE failed
to
increase the rate of swarm expansion and support the chemical
specificity of the PE response. These results also suggest that
directed movement is at least partly due to enhancement of cell
velocity. A preferable way to measure chemotaxis and chemokinesis
is to
measure the reversal frequency and cellular speed of individual
cells
in response to PE. However, microscopic analysis of cell
movement has
proven difficult, as twitching
P. aeruginosa is motile
only
in groups, and hence individuals are obscured by their neighbors.
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FIG. 3.
P. aeruginosa twitching rate increased in the
presence of uniform concentrations of some synthetic PE. The rate of
PAO1 swarm expansion was measured when cells were spotted directly on
top of the PE source. The following synthetic PEs were tested:
dilauroyl PE ( ), dimyristoyl PE ( ), dipalmitoyl PE ( ),
diheptadecanoyl PE ( ), distearoyl PE ( ), and dioleoyl PE ( ).
Each point represents the average of three measurements.
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|
The results presented here suggest that PE acts as a transduced
stimulus to influence
P. aeruginosa twitching motility, but
the mechanism of signal transduction is not known. While it is
interesting that PilJ is homologous to a methyl-accepting chemotaxis
protein chemoreceptor, the complete lack of pili and twitching
motility
in a
pilJ mutant prohibits any conclusions concerning
the
role of this system in sensory transduction. Directly upstream
of
pilJ in the
P. aeruginosa chromosome lie
pilG,
pilH, and
pilI,
homologues of
enteric
cheY, another
cheY gene, and
cheW (chemotaxis
genes), respectively (
8).
Although
pilG and
pilI mutants have
the same
twitching-deficient phenotype as
pilJ mutants,
pilH mutants
express type IV pili but produce
doughnut-shaped swirls on an
agar surface, suggesting that control of
twitching motility is
dramatically altered (
8). Since
pilH is homologous to genes
required for enteric chemotaxis
and a
pilH mutant has altered
surface motility behavior, we
wanted to examine the
pilH mutant
response to PE gradients.
This mutant demonstrated no swarm expansion
whatsoever in our assays.
In fact, microscopic examination of
the agar surface revealed extensive
lysis; it appears that the
starvation conditions of the assay are
lethal to the
pilH mutant.
The
pilH mutant could
be very helpful in determining the role
of these
che
homologues in PE signal transduction, but it unfortunately
remained
intractable under the assay conditions of this
study.
The recent publication of the
P. aeruginosa PAO1 genome
sequence revealed four complete chemotaxis-like signal transduction
systems, indicating an enormous complexity in motility control
(
26). One system controls swimming chemotaxis
(
17), and the
pil system is essential for
twitching (
8), but the other two
systems are novel and
their roles are not understood. It is interesting
that the third system
is most related to that found in
R. sphaeroides,
an organism
which responds chemokinetically to some chemicals
(
23),
while the fourth system is homologous to the
M. xanthus frz
system, which controls gliding behavior and is involved in
adaptation
to PE during chemotaxis (
3,
18). It will be interesting
to
determine the effects of mutations in the
R. sphaeroides-
and
M. xanthus-like signal transduction systems on twitching
motility
and the response to PE. It is also worth noting that Foster et
al. have suggested that type IV pili of enteropathogenic
E. coli may bind PE directly (
10). Perhaps PE binding to
type IV pili
increases either the rate or the force of pilus
retraction.
Lipids are ideal signals for surface-borne organisms, as they adhere to
surfaces and diffuse slowly. That
P. aeruginosa biases
twitching motility up PE gradients lends further support to the
idea
that surface-motile organisms utilize lipids as chemoeffectors.
PE
could conceivably regulate motility during
M. xanthus
fruiting-body
formation and
P. aeruginosa biofilm
microcolony aggregation, as
both processes are dependent on type IV
pili (
22). PE from
P. aeruginosa membranes is
active, suggesting that it may serve as
an endogenous autoattractant
and aggregation signal. It is also
possible that
P. aeruginosa might also direct twitching toward
PE from host cells
and use these signals for orientation during
infection. Twitching
motility has been identified in a variety
of pathogenic organisms,
including
Acinetobacter calcoaceticus,
Neisseria
gonorrhoeae,
Neisseria meningitidis,
Moraxella
bovis,
and
Pasteurella multocida (
13,
14).
Enteropathogenic
E. coli may also possess twitching
motility, as mutants deficient in type
IV pilus production lack
localized adherence or microcolony formation
and are dramatically
reduced in virulence (
2). It is interesting
to speculate
that type IV pilus-dependent surface motility directed
by lipid
effectors may be a critical event in pathogenesis in
these and other
organisms.
| |
ACKNOWLEDGMENTS |
This work was supported by grant MCB9601077 from the NSF and a
Grant-in-Aid of Research from the National Academy of Sciences through
Sigma Xi, The Scientific Research Society.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology, 527 Biological Sciences Building, University of Georgia, Athens, GA 30602. Phone: (706) 542-2681. Fax: (706) 542-2674. E-mail:
shimkets{at}arches.uga.edu.
| |
REFERENCES |
| 1.
|
Berg, H. C., and D. A. Brown.
1972.
Chemotaxis in Escherichia coli analysed by three-dimensional tracking.
Nature
239:500-504[CrossRef][Medline].
|
| 2.
|
Bieber, D.,
S. W. Ramer,
C. Y. Wu,
W. J. Murray,
T. Tobe,
R. Fernandez, and G. K. Schoolnik.
1998.
Type IV pili, transient bacterial aggregates, and virulence of enteropathogenic Escherichia coli.
Science
280:2114-2118[Abstract/Free Full Text].
|
| 3.
|
Blackhart, B. D., and D. R. Zusman.
1985.
"Frizzy" genes of Myxococcus xanthus are involved in control of frequency of reversal of gliding motility.
Proc. Natl. Acad. Sci. USA
82:8767-8770[Abstract/Free Full Text].
|
| 4.
|
Bligh, E. G., and W. J. Dyer.
1959.
A rapid method of total lipid extraction and purification.
Can. J. Biochem. Physiol.
37:911-917.
|
| 5.
|
Borkovich, K. A.,
L. A. Alex, and M. I. Simon.
1992.
Attenuation of sensory receptor signaling by covalent modification.
Proc. Natl. Acad. Sci. USA
89:6756-6760[Abstract/Free Full Text].
|
| 6.
|
Bradley, D. E.
1980.
A function of Pseudomonas aeruginosa PAO polar pili: twitching motility.
Can. J. Microbiol.
26:146-154[Medline].
|
| 7.
|
Costerton, J. W.,
Z. Lewandowski,
D. E. Caldwell,
D. R. Korber, and H. M. Lappin-Scott.
1995.
Microbial biofilms.
Annu. Rev. Microbiol.
49:711-745[CrossRef][Medline].
|
| 8.
|
Darzins, A.
1994.
Characterization of a Pseudomonas aeruginosa gene cluster involved in pilus biosynthesis and twitching motility: sequence similarity to the chemotaxis proteins of enterics and the gliding bacterium Myxococcus xanthus.
Mol. Microbiol.
11:137-153[CrossRef][Medline].
|
| 9.
|
Davies, D. G.,
M. R. Parsek,
J. P. Pearson,
B. H. Iglewski,
J. W. Costerton, and E. P. Greenberg.
1998.
The involvement of cell-to-cell signals in the development of a bacterial biofilm.
Science
280:295-298[Abstract/Free Full Text].
|
| 10.
|
Foster, D. B.,
D. Philpott,
M. Abul-Milh,
M. Huesca,
P. M. Sherman, and C. A. Lingwood.
1999.
Phosphatidylethanolamine recognition promotes enteropathogenic E. coli and enterohemorrhagic E. coli host cell attachment.
Microb. Pathog.
27:289-301[CrossRef][Medline].
|
| 11.
|
Guoyong, L., and R. M. Weis.
2000.
Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli.
Cell
100:357-365[CrossRef][Medline].
|
| 12.
|
Hamilton, J. G., and K. Comai.
1988.
Rapid separation of neutral lipids, free fatty acids and polar lipids using prepacked silica sep-pak columns.
Lipids
23:1146-1149[Medline].
|
| 13.
|
Henrichsen, J.
1975.
The occurrence of twitching motility among Gram-negative bacteria.
Acta Pathol. Microbiol. Scand. Sect. B
83:171-178[Medline].
|
| 14.
|
Henriksen, S. D., and L. O. Frøholm.
1975.
A fimbriated strain of Pasteurella multocida with spreading and corroding colonies.
Acta Pathol. Microbiol. Scand. Sect. B
83:129-132[Medline].
|
| 15.
|
Jennings, W. G.
1994.
Lipids, p. 245-285.
In
F. Bernard, and J. Sherma (ed.), Thin layer chromatography: techniques and applications, 3rd ed. Marcel Dekker Inc., New York, N.Y.
|
| 16.
|
Kaiser, D., and C. Crosby.
1983.
Cell movement and its coordination in swarms of Myxococcus xanthus.
Cell Motil.
3:227-245[CrossRef].
|
| 17.
|
Kato, J.,
T. Nakamura,
A. Kuroda, and H. Ohtake.
1999.
Cloning and characterization of chemotaxis genes in Pseudomonas aeruginosa.
Biosci. Biotechnol. Biochem.
63:155-161[CrossRef][Medline].
|
| 18.
|
Kearns, D. B., and L. J. Shimkets.
1998.
Chemotaxis in a gliding bacterium.
Proc. Natl. Acad. Sci. USA
95:11857-11962.
|
| 19.
|
Lam, J.,
R. Chan,
K. Lam, and J. W. Costerton.
1980.
Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis.
Infect. Immun.
28:546-556[Abstract/Free Full Text].
|
| 20.
|
Merz, A. J.,
M. So, and M. P. Sheetz.
2000.
Pilus retraction powers bacterial twitching motility.
Nature
407:98-102[CrossRef][Medline].
|
| 21.
|
Nunn, D.,
S. Bergman, and S. Lory.
1990.
Products of three accessory genes, pilB, pilC, and pilD, are required for biogenesis of Pseudomonas aeruginosa pili.
J. Bacteriol.
172:2911-2919[Abstract/Free Full Text].
|
| 22.
|
O'Toole, G. A., and R. Kolter.
1998.
Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development.
Mol. Microbiol.
30:295-304[CrossRef][Medline].
|
| 23.
|
Packer, H. L.,
D. E. Gauden, and J. P. Armitage.
1996.
The behavioral response of anaerobic Rhodobacter sphaeroides to temporal stimuli.
Microbiology
142:593-599[Abstract/Free Full Text].
|
| 24.
|
Semmler, A. B. T.,
C. B. Whitchurch, and J. S. Mattick.
1999.
A re-examination of twitching motility in Pseudomonas aeruginosa.
Microbiology
145:2863-2873[Abstract/Free Full Text].
|
| 25.
|
Shimkets, L. J.
1990.
Social and developmental biology of the myxobacteria.
Microbiol. Rev.
54:473-501[Abstract/Free Full Text].
|
| 26.
|
Stover, C. K.,
X. Q. Pham,
A. L. Erwin,
S. D. Mizoguchi,
P. Warrener,
M. J. Hickey,
F. S. L. Brinkman,
W. O. Hufnagle,
D. J. Kowalik,
M. Lagrou,
R. L. Garber,
L. Goltry,
E. Tolentino,
S. Westbrook-Wadman,
Y. Yaun,
L. L. Brody,
S. N. Coulter,
K. R. Folger,
A. Kas,
K. Larbig,
R. Lim,
D. Spencer,
G. K.-S. Wong,
Z. Wu,
I. T. Paulsen,
J. Reizer,
M. H. Saier,
R. E. W. Hancock,
S. Lory, and M. V. Olson.
2000.
Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen.
Nature
406:959-964[CrossRef][Medline].
|
| 27.
|
Van Delden, C., and B. H. Iglewski.
1998.
Cell-to-cell signaling and Pseudomonas aeruginosa infections.
Emerg. Infect. Dis.
4:551-560[Medline].
|
| 28.
|
Ward, M. J.,
K. C. Mok, and D. R. Zusman.
1998.
Myxococcus xanthus displays Frz-dependent chemokinetic behavior during vegetative growth.
J. Bacteriol.
180:440-443[Abstract/Free Full Text].
|
Journal of Bacteriology, January 2001, p. 763-767, Vol. 183, No. 2
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.2.763-767.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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-
Miller, R. M., Tomaras, A. P., Barker, A. P., Voelker, D. R., Chan, E. D., Vasil, A. I., Vasil, M. L.
(2008). Pseudomonas aeruginosa Twitching Motility-Mediated Chemotaxis towards Phospholipids and Fatty Acids: Specificity and Metabolic Requirements. J. Bacteriol.
190: 4038-4049
[Abstract]
[Full Text]
-
Wilhelm, S., Gdynia, A., Tielen, P., Rosenau, F., Jaeger, K.-E.
(2007). The Autotransporter Esterase EstA of Pseudomonas aeruginosa Is Required for Rhamnolipid Production, Cell Motility, and Biofilm Formation. J. Bacteriol.
189: 6695-6703
[Abstract]
[Full Text]
-
Sonawane, A., Jyot, J., Ramphal, R.
(2006). Pseudomonas aeruginosa LecB Is Involved in Pilus Biogenesis and Protease IV Activity but Not in Adhesion to Respiratory Mucins. Infect. Immun.
74: 7035-7039
[Abstract]
[Full Text]
-
Scher, K., Romling, U., Yaron, S.
(2005). Effect of Heat, Acidification, and Chlorination on Salmonella enterica Serovar Typhimurium Cells in a Biofilm Formed at the Air-Liquid Interface. Appl. Environ. Microbiol.
71: 1163-1168
[Abstract]
[Full Text]
-
Szurmant, H., Ordal, G. W.
(2004). Diversity in Chemotaxis Mechanisms among the Bacteria and Archaea. Microbiol. Mol. Biol. Rev.
68: 301-319
[Abstract]
[Full Text]
-
Ferrandez, A., Hawkins, A. C., Summerfield, D. T., Harwood, C. S.
(2002). Cluster II che Genes from Pseudomonas aeruginosa Are Required for an Optimal Chemotactic Response. J. Bacteriol.
184: 4374-4383
[Abstract]
[Full Text]
-
Schmitt, R.
(2002). Sinorhizobial chemotaxis: a departure from the enterobacterial paradigm. Microbiology
148: 627-631
[Full Text]
-
Khursigara, C., Abul-Milh, M., Lau, B., Giron, J. A., Lingwood, C. A., Foster, D. E. B.
(2001). Enteropathogenic Escherichiacoli Virulence Factor Bundle-Forming Pilus Has a Binding Specificity for Phosphatidylethanolamine. Infect. Immun.
69: 6573-6579
[Abstract]
[Full Text]
-
Skerker, J. M., Berg, H. C.
(2001). Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA
10.1073/pnas.121171698v1
[Abstract]
[Full Text]
-
Skerker, J. M., Berg, H. C.
(2001). Direct observation of extension and retraction of type IV pili. Proc. Natl. Acad. Sci. USA
98: 6901-6904
[Abstract]
[Full Text]
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