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Journal of Bacteriology, July 2001, p. 4210-4216, Vol. 183, No. 14
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.14.4210-4216.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Indole Can Act as an Extracellular Signal in
Escherichia coli
Dandan
Wang,1
Xuedong
Ding,1 and
Philip N.
Rather1,2,*
Departments of Medicine and Molecular Biology and
Microbiology, Case Western Reserve University School of
Medicine,1 and Research Service,
Veterans Affairs Medical Center,2 Cleveland,
Ohio 44106
Received 25 January 2001/Accepted 26 April 2001
 |
ABSTRACT |
Previous work has shown that lacZ fusions to the
cysK, astD, tnaB, and gabT genes in
Escherichia coli are activated by self-produced extracellular signals. Using a combination of ethyl acetate extraction, reversed-phase C18 chromatography, and thin-layer
chromatography, we have purified an extracellular activating signal
from E. coli supernatants. Mass spectrometry revealed a
molecule with an m/z peak of 117, consistent with indole.
Nuclear magnetic resonance analysis of the purified E. coli
factor and synthetic indole revealed identical profiles. Using
synthetic indole, a dose-dependent activation was observed with
lacZ fusions to the gabT, astD, and
tnaB genes. However,
cysK::lacZ and several control
fusions were not significantly activated by indole. Conditioned medium
prepared from a tnaA (tryptophanase) mutant, deficient in
indole production, supported 26 to 41% lower activation of the
gabT and astD fusions. The residual level of activation may be due to a second activating signal. Activation of the
tnaB::lacZ fusion was reduced by
greater than 70% in conditioned medium from a tnaA mutant.
| |
INTRODUCTION |
The use of chemical signals for
bacterial communication is a widespread phenomenon (10, 11, 20,
23, 33). In gram-negative bacteria, these signals can be
N-acyl derivatives of homoserine lactone, cyclic dipeptides,
and quinolones (3, 8, 17, 28-30, 43). In gram-positive
bacteria, small peptides appear to be the predominant signal (7,
15, 16, 18, 25, 36). In some cases, small proteins can mediate
signaling (22, 40). These signals regulate a variety of
functions, including bioluminescence, differentiation, virulence, DNA
transfer, and biofilm maturation (1, 2, 4, 5, 9, 19, 24, 27, 31,
32).
Indole production is a common diagnostic marker for the identification
of Escherichia coli (37). Among the
Enterobacteriaceae, indole is produced by E. coli
and certain members of the Proteeae, such as Proteus
vulgaris, Providencia spp., and Morganella spp. (37). Indole is formed from tryptophan by the
tryptophanase enzyme, encoded by the tnaA gene
(35). At very high concentrations (5 mM), indole is toxic
to E. coli, possibly by causing membrane changes that result
in the generation of superoxide (12). However, the
concentration at which indole is toxic is approximately 15-fold higher
than the physiological concentration seen in stationary-phase supernatants of E. coli (see below). The efflux of indole
from E. coli is mediated by the AcrEF pump, and
acrEF mutants exhibit enhanced indole sensitivity
(21). The primary pathway for indole transport into the
cell is via the Mtr permease (42).
For E. coli, the role of cell-to-cell signaling in a variety
of functions, including regulation of ftsQAZ, expression of
type III secretion systems, inhibition of DNA replication, and
activation of degradative pathways, has been described (1, 13,
34, 38, 39, 41). However, the extracellular signals involved in
these processes are poorly understood. Previous studies from our lab
have identified the E. coli genes cysK, astD,
tnaB, and gabT, which are activated by extracellular
signals (1). We have utilized a lacZ fusion to
one of these genes (gabT) as a biosensor to purify an
activating signal from E. coli supernatants. Our data
indicate that this signal is indole. In addition to the activation of
gabT, indole is also capable of activating lacZ fusions to the astD and tnaB genes, indicating
that it may affect a specific signaling pathway.
| |
MATERIALS AND METHODS |
Strains and growth conditions.
A luxS mutant of
E. coli strain DH5
, obtained from B. Bassler, Princeton
University, was used for the preparation of conditioned medium for
signal purification. Strains MT9
(cysK::lacZ), MT48 (astD::lacZ), MT113
(tnaB::lacZ), and MT114
(gabT::lacZ) have been described
previously (1). Strain TM1061 is an MC1061 derivative that
contains a tnaA::mini-Tn5 Cm null
allele and is unable to produce indole. All strains were grown in 0.5×
Luria broth (LB) at pH 7.5 for 
-galactosidase assays by the method
of Miller (26).
Bioassay conditions.
Strain MT114
gabT::lacZ was used to monitor
purification of the activating signal. Assays were conducted in 3 ml of
0.5× LB at pH 7.5, and mixtures were shaken at 280 rpm in 13- by
100-mm test tubes. Cultures were inoculated at a 1:1,000 dilution with a dilute overnight culture of MT114, and cells were harvested at an
optical density at 600 nm (OD600) of 0.35. This represented approximately 5 to 6 h of growth. The effects of indole were
examined on MT9, MT48, MT113, and MT114 using the above conditions.
Crude preparations of conditioned medium were prepared as described previously (1).
Signal purification.
For factor purification, 900 ml of LB
(three preparations of 300 ml each) was inoculated with a dilute
suspension of log-phase DH5 and allowed to shake overnight at 300 rpm. Cells were harvested at an A600 of 1.5 and
were pelleted by centrifugation at 4,300 × g. The
resulting supernatant was filter sterilized, and the pH was adjusted to
7.5. The supernatant was then sequentially extracted three times with
200 ml of ethyl acetate. The ethyl acetate phase was dried under a
rotary evaporator at 40°C. The material was resuspended in 1 ml of
ethyl acetate and loaded on a 5-g C18 column (Waters
Corp.). The column was washed sequentially with 20-ml portions of
H2O, 20% methanol, 50% methanol, 60% methanol, 80%
methanol, and 100% methanol. The material in the 60% wash activated
the gabT::lacZ fusion. The 60%
methanol fraction was dried on a rotary evaporator and redissolved in
300 µl of ethyl acetate. The resulting material was applied to a
silica gel thin-layer chromatography plate and eluted with hexane-ethyl
acetate (3:2). Six individual bands were typically observed, and each
band was cut out. The resulting material from each band was eluted in
ethyl acetate and tested for activity in the bioassay described above.
Structural analysis.
The high-resolution electron impact
mass spectrum was recorded on a KRATOS MS25FA spectrometer. For the
activating material, an m/z of 117.0584 was observed,
corresponding to C8H7N with a calculated value
of 117.0578. A database search of the spectrum for the activating
factor identified a match with indole. 1H nuclear magnetic
resonance (NMR) spectra in CDCl3 were recorded on a Varian
300-MHz spectrometer. The chemical shifts are reported in 
(parts
per million). The 1H NMR spectra for the activating factor
and synthetic indole (Aldrich Chemical Co. Inc.) were identical: 6.55 (m, 1H), 7.09 to 7.21 (m, 3H), 7.39 (d, J 8.1, 1H), 7.65 (d, J 7.8, 1H), 7.96 (br, s, 1H).
| |
RESULTS |
Purification of an extracellular signal that activates the
gabT::lacZ fusion.
Strain MT114
gabT::lacZ was used as a biosensor to
purify an activating signal. Previous work indicated that the
LuxS-dependent signal of E. coli was not involved in the
activation of gabT::lacZ (1). Preliminary extractions of conditioned medium
indicated that both chloroform and ethyl acetate were capable of
extracting an activating signal. However, ethyl acetate extracts gave
higher activity and were used for further experiments. The stage in
growth for optimal factor production was also examined. Although
activation of gabT::lacZ was observed
using conditioned medium from cells at mid-log phase
(A600 of 0.5), conditioned medium prepared at an
A600 of 1.5 gave the highest activity (data not shown).
To purify an activating signal, conditioned medium was prepared and
extracted with ethyl acetate as described in Materials and Methods. The
extract was applied to a reversed-phase C18 column and
eluted with increasing concentrations of methanol. The material contained within the 60% elution displayed activity when tested with
MT114 (gabT::lacZ) (data not shown).
Thin-layer chromatography of this material resulted in six prominent
bands under UV illumination. Individual bands were cut out, eluted with
ethyl acetate and tested for activity. The material from one band was
capable of activating the gabT::lacZ
fusion approximately five-fold (data not shown).
Structural analysis of the activating signal.
The
high-resolution electron impact mass spectra of the activating material
indicated a primary ion with an m/z of 117.0584 and a second
peak at an m/z of 90.04767 (Fig.
1A). A database search indicated a match
with indole (C8H7N), with an m/z of
117.0578. A comparison of the high-resolution spectrum for indole
indicated that the profile was essentially identical to that for the
activating signal (Fig. 1B). NMR analysis was then used to further
confirm the chemical nature of the activating signal. The
1H NMR spectra of the activating signal (Fig.
2A) and synthetic indole (Fig. 2B)
revealed identical profiles. In addition, the purified activating
material gave an intense purple reaction with Kovács reagent.
These data taken together indicate that the activating factor is
indole.
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FIG. 1.
Electron impact mass spectra of the activating fraction
(A) and of synthetic indole (B). The m/z peaks were 117.0584 (C8H7N; calculated, 117.0578) and 90.04767 (C7H6-CHN+).
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FIG. 2.
1H NMR spectra of the activating factor and
synthetic indole. The chemical shifts are reported in (ppm)
relative to residual trimethyl silane. The 1H NMR spectra
for the activating factor (A) and synthetic indole (B) were identical
(see Materials and Methods).
|
|
The concentration of extracellular indole produced by
E. coli has previously been reported at 150 µM in minimal medium
supplemented
with tryptophan (
12). However, we have
observed that stationary-phase
LB cultures of MG1655 have an indole
concentration of 340 µM.
Synthetic indole activates the astD, tnaB, and
gabT fusions in a dose-dependent manner.
To confirm
the identification of indole as an activating molecule, synthetic
indole was tested for the ability to prematurely activate various
quorum-sensing regulated lacZ fusions at early log phase. In
Fig. 3, the effects of indole on
-galactosidase expression from each fusion are shown. The
cysK::lacZ fusion (MT9) was not
significantly activated by indole, with a 1.7-fold activation seen at 1 mM. In contrast, lacZ fusions to astD (MT48),
tnaB (MT113), and gabT (MT114) were activated
4.3-, 8.3-, and 4.0-fold, respectively, at a concentration of 1 mM
indole (Fig. 4). At 2 mM indole, the astD (MT48), tnaB (MT113), and gabT
(MT114) fusions were activated 7.6-, 9.6-, and 6.6-fold, respectively.
Indole did not stimulate growth, and at a concentration of 2 mM, it
resulted in slower growth of MT48, MT113, and MT114. At 2 mM indole,
MT9 was unable to reach an OD of 0.35. As a control, we examined the
effects of indole at 1 mM on the expression of a random,
uncharacterized lacZ fusion to a non-quorum-sensing
activated gene. This fusion was not significantly activated and
exhibited an induction value of 1.2-fold (data not shown). In addition,
the expression of lacZ from its native chromosomal location
in MG1655 was not altered by indole at 1 or 2 mM (data not shown).
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FIG. 3.
Effects of indole on expression. The effects of
synthetic indole on expression of lacZ fusions to
cysK (MT9), atsD (MT48), tnaB (MT113),
and gabT (MT114) were monitored by -galactosidase
expression (Miller units). Average results from duplicate experiments
are shown. Standard deviations were less that 10% for each value.
Duplicate experiments gave results similar to those shown.
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FIG. 4.
Possible model for indole signaling in E. coli. The tnaAB operon is depicted and is activated by
CRP-cAMP as nutrients are depleted. This results in indole production
via the TnaA (tryptophanase) enzyme. The indole is secreted and acts as
an extracellular signal. The components of the signal response pathway
are unknown and are indicated by a question mark.
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|
Altered activation by conditioned medium from a tnaA
(tryptophanase) mutant.
The production of indole from tryptophan
depends on the tryptophanase enzyme (TnaA) (35). We
investigated the role of secreted indole in conditioned medium on the
activation of the fusions. Conditioned medium was prepared from MC1061
(wild type) and the isogenic derivative TM1061
(tnaA::mini-Tn5Cm) at an
OD600 of 1.6 and was tested for the ability to activate
lacZ fusions to the cysK, astD, tnaB, and
gabT genes (Table 1). The
TM1061 strain produced levels of indole that were below detection by
standard methods (12). For the cysK (MT9),
astD (MT48), and gabT(MT114) fusions, the
activation values with conditioned medium from TM1061 were lower by 27, 41, and 26%, respectively, than the activation values with conditioned
medium from MC1061 (wild type). For the tnaB fusion (MT113),
the activation was lower by 70% with conditioned medium from TM1061,
relative to MC1061 (Table 1).
The ability of indole at physiologically relevant concentrations to
restore full activation of indole-deficient conditioned
medium from the
tnaA mutant was examined with the
tnaB and
gabT fusions (Table
2). Using
tnaA
mutant-conditioned medium supplemented
with indole at 300 µM, the
expression of
-galactosidase from
the
tnaB::
lacZ and
gabT::
lacZ fusions was restored to a
level
that was 92 and 115%, respectively, of the levels with
wild-type-conditioned
medium (Table
2).
With indole supplementation at 600 µM, the
restored expression of
-galactosidase for the
tnaB and
gabT fusions
corresponded to 116 and 127%, respectively, of the levels with
wild-type-conditioned medium.
| |
DISCUSSION |
Previous studies of gram-negative bacteria have shown that the
primary signaling molecules involved in cell-cell communication are
N-acyl derivatives of homoserine lactone, cyclic peptides, and quinolones (10, 11, 17, 29, 33). In this study, we
have demonstrated that indole can act as an extracellular signaling molecule and activate the astD, tnaB, and gabT
genes in a concentration-dependent manner. To date, there is no direct
evidence that E. coli produces any of the N-acyl
homoserine lactone signals commonly used in other gram-negative
bacteria. Therefore, E. coli may have evolved to utilize
alternative signals, such as the accumulation of certain metabolites.
Signaling via metabolites may allow cells to fine-tune the regulation
of target genes in response to changing environmental conditions. In
addition, signaling by indole may not be limited to E. coli,
as indole induces spore formation in the myxobacterium Stigmatella aurantiaca (14).
In E. coli, the addition of synthetic indole activated the
astD, tnaB, and gabT fusions but did not activate
cysK::lacZ or several control
lacZ fusions. The use of a tnaA null mutant
demonstrated that conditioned medium lacking indole exhibited a reduced
ability to activate these fusions, relative to wild-type-conditioned
medium (Table 1). In the case of
cysK::lacZ, which is not activated by
indole, it is unclear why conditioned medium from a tnaA
mutant supported a lower level of activation. One possibility is that production of the signal for cysK activation is indirectly
coupled to the activity of tryptophanase.
For the tnaB fusion, indole appears to be the primary
extracellular signal required for activation, as conditioned medium lacking indole exhibited a 70% reduction in tnaB
activation. Previous studies by Yanofsky et al. reported that indole
was not able to induce expression of the tna operon
(42). We have obtained SVS1144 tnaA'-'lacZ, used by Yanofsky et al., and found
that it is induced by indole during growth in LB. The use of different
media and/or indole concentrations could account for the differences in
our results.
With the astD and gabT fusions, there was
significant residual activation with conditioned medium lacking indole
(Table 1). In addition, the concentration of synthetic indole required
for activation of the astD and gabT fusions in LB
only was above 500 µM, a concentration higher than the 340 µM that
we have observed in stationary-phase E. coli supernants.
However, when indole was added back to conditioned medium from a
tnaA mutant lacking indole, the level of
gabT::lacZ activation could be restored
to wild-type levels with physiologically relevant concentrations of
indole (300 µM). In light of these results, we propose that a second extracellular signal is produced by E. coli and that the
combination of both signals is required for full activation of
gabT and possibly astD.
In Fig. 4, a model that represents a possible physiological role for
signaling by indole is presented. The initial component of this model
is the tnaAB operon, which is activated by cyclic AMP
receptor protein-cyclic AMP complex (CRP-cAMP) (6). We hypothesize that nutrient depletion during the increase in cell density
is the initial trigger that activates tnaAB via CRP-cAMP. This activation is predicted to result in an increase in indole production. In support of this model, our preliminary studies indicate
that the concentration of extracellular indole increases when cells are
starved at low cell density. The intracellular indole is then exported
by the AcrEF efflux system (21) to the outside of the
cell, where it accumulates in the growth medium. At this time, the
components of the indole response pathway are unknown. The signaling
pathway may involve the Mtr permease, which transports indole into the
cell (42). The net result of this putative signaling
pathway is predicted to be a positive amplifying loop for indole
production via the tnaAB operon.
Two targets of indole-mediated signaling are the astD and
gabT genes. These genes function in pathways that degrade
amino acids to pyruvate or succinate (1). Furthermore,
tryptophanase enzyme (TnaA) is able to catabolize tryptophan, cysteine,
and serine to pyruvate (35). Studies by Zinser and Kolter
have shown that the ability to catabolize amino acids is an important
parameter in the ability to persist and compete in stationary phase
(44). This raises the possibility that signaling by indole
may play a role in a pathway which prepares the cells for a
nutrient-poor environment when the catabolism of amino acids becomes
important for energy production.
| |
ACKNOWLEDGMENT |
This work was funded by National Science Foundation award MCB9904766.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Division of
Infectious Diseases, BRB-10, Case Western Reserve University, School of Medicine, 10900 Euclid Ave., Cleveland, OH 44106. Phone: (216) 368-0733. Fax: (216) 368-2034. E-mail:
pxr17{at}po.cwru.edu.
| |
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Journal of Bacteriology, July 2001, p. 4210-4216, Vol. 183, No. 14
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.14.4210-4216.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
