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Journal of Bacteriology, October 2001, p. 6135-6139, Vol. 183, No. 20
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.20.6135-6139.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Glycerol 3-Phosphate Inhibits Swarming and
Aggregation of Myxococcus xanthus
Aurelio
Moraleda-Muñoz,
Juana
Carrero-Lérida,
Antonio L.
Extremera,
José M.
Arias, and
José
Muñoz-Dorado*
Departamento de Microbiología,
Facultad de Ciencias, Universidad de Granada, Granada, Spain
Received 29 January 2001/Accepted 18 July 2001
 |
ABSTRACT |
We have cloned a gene of Myxococcus xanthus with
similarities to the permease for glycerol 3-phosphate (G3P) of other
bacteria. Expression of the gene increased significantly during the
first hours of starvation. Swarming of the wild-type strain was
inhibited and aggregation was delayed by G3P. Conversely, a
glpT strain aggregated even on rich medium. These
results indicate that G3P may function to regulate the timing of
aggregation in M. xanthus.
| |
TEXT |
Myxococcus xanthus is a
soil-dwelling bacterium that exhibits a complex developmental cycle
upon starvation. After depletion of nutrients, cells migrate by gliding
on a solid surface and pile up at certain points, where they create
colored macroscopic structures known as fruiting bodies. Inside, the
cells differentiate into dormant cells, the myxospores, which are
resistant to several extreme environmental conditions (4).
A decade ago, it was found that M. xanthus possesses a
family of eukaryotic-type protein serine/threonine kinases
(28). Several protein kinases have been characterized
(8, 18, 23, 27). These findings have revealed that
phosphorylation of certain proteins must be an important event in the
regulation of the developmental cycle. We reasoned that there must be
other proteins that dephosphorylate the substrates phosphorylated by
the kinases, reversing their action. These proteins will have
phosphatase activity.
In order to identify and isolate genes that encode phosphatases, we
constructed a library of M. xanthus DZF1 chromosomal DNA partially digested with Sau3AI (fragments of 3 to 4 kb) in
pUC19 (25) digested with BamHI and
dephosphorylated. The library thus constructed was used to transform
Escherichia coli DH5 (7), and positive strains
were selected on Luria-Bertani (LB) medium (16) containing
50 µg of ampicillin and 40 µg of 5-bromo-4-chloro-3-indolyl phosphate (BCIP) per ml. Because BCIP is a substrate for phosphatases, positive colonies should exhibit a blue color.
After analyzing more than 20,000 clones, 23 blue colonies were
obtained. One of the clones was sequenced using the dideoxy terminator
method (21) in an Applied Biosystems 373 DNA sequencer. Appropriate oligonucleotides were designed as primers. Analysis of the
sequence revealed that this clone contained an open reading frame (ORF)
with 96% of the codons using either G or C as the third base, a
peculiarity of M. xanthus genes (12). The
initiation codon was identified based on the observation that it is the
first ATG that occurs after a termination codon in the same reading frame. In addition, a putative ribosome-binding site (AGAGG) is located
seven bases upstream of the initiation codon. This ORF encoded a
protein with a molecular weight of 51,736.
Comparison of the protein with others in the database by using the
FASTA program, version 3.3t06 (20), revealed that it was
very similar to the permease for glycerol 3-phosphate (G3P) of other
bacteria. For that reason, the gene was designated glpT. The
M. xanthus GlpT protein exhibits 25.4% identity with the
permease of Bacillus subtilis (19) and 24.6%
with that of Vibrio cholerae (9). The
respective similarities are as high as 40% if functionally similar
amino acids are considered. This homology extended throughout the
protein. M. xanthus GlpT is also a very hydrophobic protein, and as many as 12 stretches of amino acids that can potentially function as transmembrane domains were observed. It should be noted
that other GlpT proteins also contain 12 transmembrane domains (5). The nucleotide sequence of the glpT gene
has been deposited in the GenBank database with accession number
AF157828
glpT is developmentally regulated.
In order to
examine the temporal expression of the glpT gene, a strain
bearing an M. xanthus glpT promoter fusion to the E. coli lacZ gene was constructed. A BamHI site was
created in the glpT gene by PCR using the primer
5'-CCAGGGATCCAGCGACGACATGCAGC-3', which anneals at positions
839 to 864, and the reverse primer 5'-AAACAGCTATGACCATG-3',
which anneals at the vector. The 0.85-kb amplified fragment was
digested with XbaI and BamHI and ligated to
pBluescript SK+ digested with the same enzymes. The plasmid
thus obtained was designated pBS17Bam. This plasmid was sequenced to
confirm that the BamHI site created in glpT was
in the same reading frame as the BamHI site of the
lacZ gene in plasmid pKM005 (15). Plasmid pBS17Bam was digested with XbaI and BamHI, and
the 0.85-kb fragment was ligated to pKM005 digested with the same
enzymes. The resulting plasmid was designated pGLPZY. Finally, the
kanamycin resistance gene was obtained by digestion of
pUC7Skm(Pst
) (kindly provided by S. Inouye, University of
Medicine and Dentistry of New Jersey) with SalI, and the
1.3-kb fragment was inserted into the unique SalI site of
pGLPZY. This final plasmid, pGLPZYkan, was introduced into M. xanthus by electroporation (13).
Several kanamycin-resistant colonies were analyzed by Southern blot
hybridization to confirm that they bore the fusion. DNA probes were
labeled with digoxigenin, and hybridization was carried out at 42°C
in 50% formamide under the conditions reported previously (11). A kit for color detection with Nitro Blue
Tetrazolium-BCIP was used. The strain thus obtained was designated
glpZY. The glpZY strain was then plated in
several media containing different concentrations of nutrients, and
-galactosidase activity was quantified using ONPG
(o-nitrophenyl--D-galactopyranoside) as a
substrate, as previously described (14).
For the preparation of cell extracts, several 20-µl drops of
concentrated cultures containing 2 × 10
10 cells/ml
were spotted on the appropriate medium, either CTT (
10),
1/2CTT (identical to CTT medium but containing only half as much
Bacto-Casitone), or CF agar (
6). After incubation, cells
were
harvested by scraping off the cells on the surface of the plates.
Vegetative cells were then resuspended in 200 µl of TM buffer
(10 mM
Tris-HCl [pH 7.5], 8 mM MgSO
4) and disrupted by
sonication.
Fruiting bodies were resuspended in 200 µl of glass beads
equilibrated
in TM buffer and sonicated as described previously
(
18). After
sonication, cell debris was removed by
centrifugation. The amount
of protein in the supernatants was
determined by using the Bio-Rad
protein
assay.
As shown in Fig.
1, on rich media (CTT
and 1/2CTT), initial levels of
-galactosidase activity were quite
high and then decreased
slowly with incubation. In contrast, on CF
medium, the levels
of
-galactosidase activity increased immediately
after spotting
reaching a maximum at 8 h. Later, expression
dropped until it
reached the same level as observed for vegetative
growth again.
Hence, it can be concluded that
glpT is
expressed during vegetative
growth, but its level of expression
increases at the onset of
development.
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FIG. 1.
Analysis of expression of the glpT gene in
CTT ( ), 1/2CTT ( ), and CF ( ) agar media. -Galactosidase
specific activity is expressed as nanomoles of ONP produced per
milligram of protein in 1 min. The results shown are the average of
three experiments.
|
|
G3P inhibits swarming and aggregation of M. xanthus.
The effect of the addition of several
concentrations of G3P to different culture media on the vegetative
growth and development of the wild-type strain was also analyzed. The
most evident effect of G3P on M. xanthus was a reduction of
the swarming ability of the bacterium. A decrease in the diameter of
the drops after incubation correlated with increasing concentration of
G3P in all of the media tested. This inhibition was especially
pronounced on rich media. As an example, the diameter of the drops
after 1 week of incubation at 30°C on CTT medium containing 4 mM G3P
was 11 mm, while the diameter observed on CTT with no G3P added was 20 mm (the original diameter of the drops was approximately 6 mm). On CF
medium, on which M. xanthus follows the developmental cycle, the effect on swarming is not as dramatic (the diameter of the drops
was reduced only from 12 to 9 mm on a medium containing 4 mM G3P).
However, it was clearly observed that aggregation and fruiting body
formation on CF medium containing G3P was delayed (Fig.
2). The addition of 1 mM G3P delayed
aggregation by approximately 8 h, 2 mM G3P by 24 h, and 5 mM
G3P by more than 3 days (Fig. 2). In the presence of 5 mM G3P, the
fruiting bodies appeared quite abnormal and transparent (Fig. 2),
although they contained myxospores (data not shown).
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FIG. 2.
Effect of G3P on aggregation and fruiting body formation
of the M. xanthus wild-type strain. Drops containing 2 × 1010 cells/ml were spotted on CF agar containing
different concentrations of G3P. Bar, 5 mm.
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|
The addition of G3P, however, did not seem to significantly affect
sporulation. Comparison of the number of myxospores produced
by the
wild-type strain on CF medium containing 2 mM G3P to CF
medium
containing no G3P revealed that the timing of sporulation
was almost
identical in both media (Fig.
3).
However, the final
yield of myxospores was slightly higher in the
medium containing
G3P.
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FIG. 3.
Sporulation of wild-type strain on CF agar containing 2 mM G3P ( ) or no G3P () compared with sporulation of the
glpT strain on CF agar without G3P (). The results
shown are the average of three experiments. Ten drops (20 µl each)
were spotted on an 9-cm petri dish containing CF agar. At different
times, the fruiting bodies from one plate were harvested and
resuspended in 200 µl of TM buffer. Fruiting bodies were dispersed,
and rod-shaped cells were disrupted by sonication. Myxospores were
counted in a Petroff-Hausser chamber.
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|
Phenotype of a glpT strain.
In order to study
the role of G3P during both vegetative and developmental growth, a
strain harboring a deletion in the glpT gene was
constructed. For this construction, plasmid pBS17Bam (see above) was
digested with KpnI and dephosphorylated. The linearized plasmid was then ligated to a 0.7-kb KpnI fragment, and the
orientation was checked by digestion with SmaI. The plasmid
with the correct orientation of the 0.7-kb KpnI fragment was
designated pglp. This plasmid was linearized with BamHI
and ligated to the kanamycin resistance gene obtained by digestion of
pUC7SKm(Pst) with the same enzyme. The resulting plasmid,
designated pglpkan, was linearized with SacI for
electroporation to M. xanthus. The double-crossover event
was confirmed by Southern blot hybridization.
The phenotype of the
glpT strain was analyzed. Initially,
the amount of G3P uptake by the
glpT strain was
determined. Cells
(either wild-type or
glpT strains) were
grown in liquid CTT to
an optical density at 600 nm of 1 and
centrifuged. The pellets
were resuspended in fresh liquid CTT
containing 100 µM cold G3P.
The volumes were adjusted to obtain the
same optical density (0.7)
for all the samples. The experiment was
started by the addition
of 10 µl of
L-[U-
14C]G3P per ml of culture. After 6 h of incubation, aliquots (100
µl) were withdrawn and diluted in 1 ml
of fresh liquid CTT. These
samples were immediately filtered through a
0.45-µm-pore-size
nitrocellulose membrane (Millipore), and the
membranes were washed
with 10 ml of liquid CTT. Membranes were then
dried and dissolved
with 200 µl of ethylene glycol monomethyl ether.
Radioactivity
bound to the filter was measured by liquid scintillation
counting.
The results revealed that the 10
8 cells of the wild-type
strain incorporated 436.37 ± 10.64 pmol in 1 h. In contrast,
the same
number of cells of the deletion strain incorporated
370.50 ± 7.10
pmol in the same time. The deletion of the
glpT gene does not
abolish the uptake of G3P in
M. xanthus. This result is not surprising,
because it is known that
other bacteria possess an alternative
transport system to introduce
G3P, the
ugp system (
1,
22).
While such a
system has not been reported in
M. xanthus, our results
indicate that this bacterium must have other permeases responsible
for
the uptake of approximately 85% of the total G3P that cells
can
incorporate.
The phenotype of the deletion strain grown on solid 1/2CTT and CF media
was also analyzed. On 1/2CTT agar, fruiting bodies
of the
glpT strain were clearly observed after only 24 h of
incubation
(Fig.
4). These fruiting
bodies were very stable on this medium,
and although they appeared
initially in the center of the drops,
later they also appeared in the
newly colonized area (Fig.
4).
The morphology and opacity of the
fruiting bodies were very similar
to those obtained on CF agar, and
they were full of spores.
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FIG. 4.
Phenotype of glpT strain on 1/2CTT medium
compared with wild-type strain. Cells were grown in liquid CTT at
approximately 3 × 108 cells/ml and concentrated to
2 × 1010 cells/ml in TM buffer. One drop (10 µl)
was spotted in the center of a petri dish (5.5 cm) containing 1/2CTT
agar. Bar, 5 mm.
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|
On CF agar, the
glpT strain could also form fruiting
bodies that were very similar to those of the wild-type strain (Fig.
5), but aggregation occurred 4 to 6 h earlier in the mutant than
in the wild-type strain. After a 12-h
incubation, ripples could
be observed in the wild-type strain on the
edge of the drops.
On the contrary, the
glpT strain
formed ripples even in the center
of the drops at that time. The
glpT strain had already aggregated
at 24 h, whereas
the wild-type strain originated well-formed fruiting
bodies only on the
edge of the drop. The center of the wild-type
strain drop exhibited
incompletely defined, translucent mounds.
At 36 h of incubation,
the aggregation stage was very similar
for both strains (Fig.
5).
Another remarkable difference was that
the diameter of the drop of the
wild-type strain after 1 week
of incubation on CF agar was 12 mm, while
for the
glpT strain
the diameter was 15 mm. Both results,
faster aggregation and larger
diameter of the drops of the
glpT strain on CF agar, are exactly
opposite those
observed when the wild-type strain was spotted
on CF medium containing
G3P. In contrast, on 1/2CTT medium, the
diameter of the drops of the
glpT strain was smaller (Fig.
4).
However, it must be
taken into consideration that in this medium,
the wild-type strain grew
vegetatively while the
glpT strain
formed fruiting bodies
and spores.
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FIG. 5.
Phenotype of glpT strain on CF medium
compared with wild-type strain. The experiment was performed as
described in the legend to Fig. 4. Bar, 2 mm.
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|
The timing of sporulation and the yield of spores, on the other hand,
were similar in the mutant and the wild-type strain
(Fig.
3). These
results support our previous demonstration that
G3P inhibited
aggregation but had no significant effect on
sporulation.
The fact that the
glpT strain that we have constructed
does not exhibit a more dramatic phenotype is most likely due to its
retained ability to transport G3P. However, several differences
point
to the notion that G3P inhibits swarming and aggregation.
The addition
of G3P to the cultures, either rich or low-nutrient
media, inhibits
swarming of the wild-type strain, and therefore
the final size of the
drops after several days of incubation is
smaller in media containing
G3P. There is a direct relationship
between increasing concentrations
of G3P in the medium and the
reduction in the diameter of the drops. In
contrast, the
glpT strain can swarm further away on CF
medium. On media with low
concentrations of nutrients, such as CF, the
addition of G3P to
the medium delayed aggregation of the wild-type
strain. The
glpT strain, on the other hand, not only
formed fruiting bodies earlier
on CF medium, but also aggregated and
sporulated on a medium such
as 1/2CTT, in which the wild-type strain
does not develop. While
G3P might be used as a nutrient, so that it
delays the developmental
cycle, several lines of evidence demonstrate
that this is not
the case: (i) no significant growth on CF medium
containing G3P
was observed and (ii) sporulation took place with the
same timing
and yield of spores as in a medium with no G3P. Most
likely, the
effect of G3P on swarming and aggregation is due to an
inhibition
of gliding motility. It is possible that G3P interacts with
one
or several components of the gliding or chemiotactic
machinery.
Finally, no significant differences were observed in the levels of the
five phosphatases reported in
M. xanthus (
26)
between
the wild-type and the
glpT strains.
G3P must be produced by the activity of phospholipases on
phospholipids, the activity of which increases during the first
hours
of development (
17), a time that coincides perfectly with
the maximum levels of expression of the
glpT gene. As a
result
of the action of phospholipases, free fatty acids will appear
in
addition to G3P. These free fatty acids, known as autocides,
have been
reported to induce autolysis of
M. xanthus
(
24), and
branched-chain fatty acids constitute the E
factor, a signal whose
transmission is necessary for the completion of
the developmental
cycle (
3). This signal is produced at
5 h of starvation (
2).
Our results clearly indicate that G3P, the other product of
phospholipase activity, represents a new type of small molecule
that
somehow regulates the timing of development of
M. xanthus.
| |
ACKNOWLEDGMENTS |
We thank K. Takayama (University of New South Wales, Sydney,
Australia) for critical reading of the manuscript and S. Inouye (University of Medicine and Dentistry of New Jersey) for kindly providing plasmids and strains.
This work has been supported by the Ministerio de Educación y
Cultura, Dirección General de Enseñanza Superior, Spain
(grant numbers PB98-1359 and PB94-0781).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Departamento de
Microbiologia, Facultad de Ciencias, Universidad de Granada, Avda. Fuentenueva s/n, E-18071 Granada, Spain. Phone: 34 958 243183. Fax: 34 958 249486. E-mail: jdorado{at}ugr.es.
| |
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Journal of Bacteriology, October 2001, p. 6135-6139, Vol. 183, No. 20
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.20.6135-6139.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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