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Journal of Bacteriology, February 2000, p. 821-824, Vol. 182, No. 3
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Identification by Genetic Suppression of
Escherichia coli TolB Residues Important for TolB-Pal
Interaction
Marie-Céline
Ray,
Pierre
Germon,
Anne
Vianney,
Raymond
Portalier, and
Jean
Claude
Lazzaroni*
Unité de Microbiologie et
Génétique, UMR 5577, CNRS-INSA-Université Lyon I,
F-69622 Villeurbanne, France
Received 12 July 1999/Accepted 8 November 1999
 |
ABSTRACT |
The Tol-Pal system of Escherichia coli is involved in
maintaining outer membrane stability. Mutations in tolQ,
tolR, tolA, tolB, or
pal genes result in sensitivity to bile salts and the leakage of periplasmic proteins. Moreover, some of the tol
genes are necessary for the entry of group A colicins and the DNA of filamentous bacteriophages. TolQ, TolR, and TolA are located in the
cytoplasmic membrane where they interact with each other via their
transmembrane domains. TolB and Pal form a periplasmic complex near the
outer membrane. We used suppressor genetics to identify the regions
important for the interaction between TolB and Pal. Intragenic
suppressor mutations were characterized in a domain of Pal that was
shown to be involved in interactions with TolB and peptidoglycan.
Extragenic suppressor mutations were located in tolB gene.
The C-terminal region of TolB predicted to adopt a 
-propeller
structure was shown to be responsible for the interaction of the
protein with Pal. Unexpectedly, none of the suppressor mutations was
able to restore a correct association between Pal and peptidoglycan,
suggesting that interactions between Pal and other components such as
TolB may also be important for outer membrane stability.
| |
TEXT |
The cell envelope of gram-negative
bacteria, like Escherichia coli, acts as a barrier to the
entry of macromolecules into the cell, thus providing a protection
against the deleterious action of bacteriocins and digestive enzymes.
The envelope is composed of an outer membrane and a cytoplasmic
membrane, delimiting the periplasmic space which contains the
peptidoglycan. As a consequence, the uptake of macromolecules essential
for cell growth requires specific transport systems. For example, the
Ton system, composed of TonB and its auxiliary proteins ExbB and ExbD,
is necessary for the transport of vitamin B12 and
iron-siderophore complexes (6). Group B colicins and
bacteriophages T1 and 
80 have parasitized this system to enter the
bacterium (20). Similarly, the infection by filamentous
bacteriophages and the sensitivity to the group A colicins require some
proteins of the Tol system (12, 15, 26).
Tol proteins are located in the cell envelope and are thought to be
involved in the integration of some outer membrane components, such as
porins or lipopolysaccharides (9, 21). The
tol-pal genes map at 17 min on the E. coli
chromosome (26). They are transcribed from two adjacent
operons (25). The first operon enables the transcription of
the orf1, tolQ, tolR, and
tolA genes, whereas the second one comprises
tolB, pal, and orf2. orf1 is an open
reading frame encoding a cytoplasmic protein of unknown function
(23), and orf2 encodes a periplasmic protein
whose inactivation induces no obvious alteration in phenotype
(25). Mutations in the tol-pal genes cause the
disruption of outer membrane integrity, which is evidenced by several
phenotypes, including the release of periplasmic content, sensitivity
to bile salts, and formation of outer membrane blebs at the cell
surface (2, 17, 24). Interactions between some of the
proteins of the Tol-Pal system have been characterized. TolQ, TolR, and
TolA interact in the cytoplasmic membrane via their transmembrane
domains (8, 10, 18). The periplasmic protein TolB was shown
to interact with the outer membrane, peptidoglycan-associated proteins
OmpA, Lpp, and Pal (4, 7). Thus, TolB and Pal could be part
of a multicomponent system linking the outer membrane to peptidoglycan.
The aim of this study was to determine the regions of TolB involved in
the interaction of the protein with Pal. To this end, we used
suppressor genetic techniques which had previously allowed us to
characterize the regions of interaction between TolQ, TolR, and TolA
(10, 18). pal point mutations were identified,
and some of them involved residues important for interaction with TolB
(7). These mutations induce sensitivity to sodium cholate and release of periplasmic proteins in the medium. We used these pal mutants to search for suppressors in tolB.
Mutagenesis and search for suppressors of pal
mutations.
Strain JC7752 used in this study was an E. coli K-12 
(tolB pal) derivative of 1292 (supE
hsdS met gal lacY fhuA, provided by W. Wood). First, an in vivo
mutagenesis was performed on a mixture of cells transformed by plasmid
pJC417 derivatives (25) containing the
tolB-pal-orf2 region and carrying each of the pal mutations. Cells were grown to exponential-growth phase and were washed
in citrate buffer (0.1 M, pH 5.5). They were then incubated 10 or 20 min at 37°C in the citrate buffer containing 0.4 mg of nitrosoguanidine per ml, were washed with potassium phosphate buffer
(0.1 M, pH 7), and were shaken at 37°C for 2 h. After overnight growth in Luria-Bertani medium containing ampicillin, plasmids were
extracted according to the method of Birnboim and Doly (3). Strain JC7752 was transformed by the mutagenized plasmids, and cells
able to grow on plates containing 2.5% sodium cholate were selected.
Plasmids were again extracted from these strains and were reintroduced
into JC7752, in order to ascertain that the phenotype observed was
really due to the mutagenized plasmids. The region containing the
suppressor mutation was localized by subcloning techniques and was
entirely sequenced. By using this method of screening, two extragenic
suppressor mutations were identified with the pal A88V
mutant. This mutant was previously described as having an unexpected
phenotype of tolerance towards colicin A (7), like three
other mutants (pal P94L, pal S126F, and
pal G128D). Since, unlike TolB, Pal had never been reported to be necessary for the translocation of colicin A, the phenotype observed in these four pal mutants could be due to a defect
in TolB-Pal interaction. That is why these four mutants seemed to be
good candidates for the search of extragenic suppressor mutants. Therefore, we performed a second mutagenesis on each of these four
mutants, following the same protocol as described above. Only the
mutagenesis of the plasmid carrying the pal A88V mutation led to the characterization of suppressor mutations.
Isolation of intragenic suppressor mutations of pal
A88V.
Mutations pal S99F and pal E102K were
both isolated as intragenic suppressor mutations of pal
A88V. The pal E102K mutations was previously described as a
pal-defective mutant (7). Both pal
S99F and pal E102K mutations enabled the pal A88V
mutant to grow in the presence of sodium cholate and lowered its
excretion of periplasmic enzymes, mutant pal E102K being
more efficient than mutant pal S99F as a suppressor mutation
(Table 1). Thus, the conformation of the
region from residues 88 to 102 appeared to be important for Pal
function. The region from residues 89 to 130 was shown to be able to
bind to TolB and peptidoglycan (5). Residues 97 to 114 constitute an 
-helical domain which is well conserved in all
OmpA-related proteins and has been proposed to be involved in the
association of these proteins with peptidoglycan (14). The
suppression observed could, therefore, be explained by a conformation
of Pal restoring an interaction with TolB or peptidoglycan. These two
hypotheses were tested.
Total membranes from each mutant were isolated and were then
solubilized by 2% sodium dodecyl sulfate to isolate
peptidoglycan-associated
proteins as described (
7). In such
conditions, equal amounts
of Pal were recovered in the total membrane
fraction of parental
or mutant strains (data not shown). In
pal A88V mutant and the
intragenic suppressors, Pal was not
associated with peptidoglycan,
unlike in the wild-type strain.
Therefore, the suppression could
not be due to the restoration of an
interaction with
peptidoglycan.
Mutant
pal A88V is 10-fold more tolerant towards colicins A
and E2 than is the wild-type strain (Table
1); this phenotype
is
reproducibly suppressed in both
pal double mutants. Since,
unlike TolB, Pal is not involved in the entry of colicins A and
E2,
these suppressor phenotypes may reveal a change in the conformation
of
TolB, via a modification of the TolB-Pal interaction. In mutant
pal A88V, the TolB-Pal complex could still be evidenced by
chemical
cross-linking, which was not the case for the
pal
E102K mutant
(
7). We wondered if a TolB-Pal complex could be
detected in
a
pal A88V/E102K double mutant. Cross-linking
experiments were
done on both intragenic suppressor mutants, as
described previously
(
4). An interaction between TolB and
Pal could be evidenced
in both intragenic suppressor mutants (data not
shown). Thus,
intragenic suppressor mutations appeared to lead to a
conformation
of Pal able to functionally interact with TolB. When
combined
with other
pal mutations leading to the same
colicin-tolerant
phenotype as the
pal A88V mutation, the
pal E102K mutation never
restored a wild-type phenotype.
Thus, the suppression of the
pal A88V mutation by the
pal E102K mutation was allele
specific.
Isolation of extragenic suppressor mutations of pal
A88V in tolB.
Twelve mutations affecting 11 different
residues of tolB were isolated as suppressor mutations of
pal A88V (Table 2). They enabled the pal A88V mutant to grow on plates containing
sodium cholate and lowered its excretion of periplasmic enzymes, some mutants being more efficient than others in suppressing the
pal A88V phenotype. In most cases, the tolB
mutations could not suppress the phenotypes of tolerance to colicins A
and E2 of mutant pal A88V. Three tolB point
mutations (H246Y, A249V, and T292I) affected the activity of TolB,
whereas the others had phenotypes similar to the wild type. All the
suppressor mutations were subcloned into plasmid pJC417 derivatives
carrying mutations pal P94L, pal S126F, or
pal G128D, in order to test their allele specificity. In all
cases, the tolB mutation was strictly specific of
pal A88V, because it only suppressed pal A88V
sensitivity to sodium cholate and leakage of periplasmic enzymes (data
not shown).
All the extragenic suppressor mutations of
pal A88V are
located in the C-terminal region of TolB. This suggests that this
region of TolB is important for its interaction with Pal. We already
knew that TolB and Pal could be associated in
pal A88V
mutant
(
7). Cross-linking experiments were performed in
order to verify
that TolB and Pal could also form complexes in
suppressor mutants.
This was the case in all strains (data not shown).
Therefore,
the suppressor phenotype may not be explained by the
restoration
of a TolB-Pal complex, but rather by a change in the way in
which
these two proteins interact. Interestingly, the C-terminal region
of TolB was proposed to adopt a
-propeller structure
(
19).
Similar organizations were identified in several
eukaryotic and
prokaryotic proteins, such as the large family of
proteins containing
WD repeats (
22) or the methanol
dehydrogenase from
Methylophilus methylotrophus
(
27), as well as the serine-threonine protein
kinase of
Thermonospora curvata (
13). However, the function
of
-propeller structures remains unknown. The C-terminal domain
of
E. coli TolB was shown to be composed of six repeats
organized
around a central axis, such that they could be likened to the
blades of a propeller (
19). Each repeat contains four
regions
predicted to be antiparallel
-strands, strand 4 being
outside
and strand 1 being inside (Fig.
1). The suppressor mutations of
pal A88V isolated in
tolB are located in repeats
2 to 5 and are
clustered between
-strands 2 and 3 and 4 to 1 (Fig.
1). In a
three-dimensional representation, these residues are somewhat
inside the
-propeller. The C-terminal domain of TolB could form
a
cavity into which a part of Pal could enter. The three mutants
affecting TolB activity are located between
-strands 4 and 1,
probably in a loop near the central axis, just before or at the
beginning of the inner strand. Therefore, this particular region
may
also play a role in TolB activity.
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|
FIG. 1.
Alignment of repeats found in the C-terminal domain of
E. coli TolB. The positions of residues involved in
suppressor mutations of pal A88V are shaded in black. The
four -strands are indicated above the alignment, as shown by Ponting
and Pallen (19). The consensus sequence was defined by
specific amino acids appearing more than three times at the same
position.
|
|
Here again, we checked the ability of the
tolB suppressors
to restore the association of Pal with peptidoglycan. Equal amounts
of
Pal were present in total-membrane fractions of the parental
and mutant
strains (data not shown). None of the mutants could
compensate for the
lack of association between Pal (
A88V) and
peptidoglycan. In
E. coli, other noncovalently peptidoglycan-associated
outer
membrane proteins include porins and OmpA. Mutations in
the structural
genes encoding such proteins do not lead to a phenotype
of defect in
outer membrane stability in this bacterium, indicating
that the
association between these proteins and peptidoglycan
may more reflect
an affinity between these components than an
interaction involved in
maintaining outer membrane stability.
However, this is not the case for
other OmpA-related proteins
such as
Pseudomonas aeruginosa
OprF protein which has been shown
to be involved in the maintenance of
outer membrane integrity
(
11).
Concluding remarks.
We have characterized the domains
important for the interaction between Pal and TolB and shown that the
association between Pal and peptidoglycan is not as important as
previously thought for outer membrane stability. The determination of
the tertiary structure of TolB (1) and Pal will be necessary
to identify the exact parts of both proteins which interact with each
other. It has been recently reported that, in vitro, the TolB-Pal
complex was not associated with the peptidoglycan, leading to the
conclusion that Pal may exist under two forms, one bound to TolB and
another bound to peptidoglycan (5), but we still wonder what
the real physiological significance of the Pal-peptidoglycan
association could be. The pal mutants that we isolated may
be impaired in their affinity with TolB, peptidoglycan, or both. In
addition, the existence of additional unknown factors which can also
influence the outer membrane stability cannot be excluded.
More-accurate techniques than those used in this study to characterize
the interaction between Pal, TolB, and peptidoglycan will be necessary
to determine the exact relationships between these three components
leading to the maintenance of outer membrane integrity.
| |
ACKNOWLEDGMENTS |
This work was supported by grants from the CNRS (Département
des Sciences de la Vie) and MESR. P.G. was a recipient of an AMN fellowship.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Unité de
Microbiologie et Génétique, UMR 5577, bât 405, F-69622 Villeurbanne Cedex, France. Phone: (33) 472 43 13 67. Fax: (33)
472 43 26 86. E-mail: lazzaroni{at}biomserv.univ-lyon1.fr.
| |
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Journal of Bacteriology, February 2000, p. 821-824, Vol. 182, No. 3
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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