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Journal of Bacteriology, December 1999, p. 7639-7642, Vol. 181, No. 24
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Evidence that Expression of the Vibrio
vulnificus Hemolysin Gene Is Dependent on Cyclic AMP and Cyclic
AMP Receptor Protein
Young Bae
Bang,1
Shee Eun
Lee,2
Joon Haeng
Rhee,2,3 and
Sang Ho
Choi1,3,*
Department of Food Science and Technology,
Institute of Biotechnology, Chonnam National University, Kwang-Ju,
500-757,1 and Department of
Microbiology,2 Institute of Medical
Sciences,3 Chonnam National University
Medical School, Kwang-Ju, 500-190, South Korea
Received 22 July 1999/Accepted 27 September 1999
 |
ABSTRACT |
Glucose repressed hemolysin production in Vibrio
vulnificus. Promoter activity of the hemolysin gene,
vvh, assessed with a vvh-luxCDABE
transcriptional fusion, required cyclic AMP (cAMP) and cAMP receptor
protein (CRP) in Escherichia coli. Hemolysin production in
V. vulnificus increased after the addition of cAMP and was
undetectable in a putative crp mutant, suggesting that vvh is also regulated by cAMP-CRP in V. vulnificus.
| |
TEXT |
The pathogenic marine bacterium
Vibrio vulnificus has been identified as the causative agent
of food-borne diseases such as gastroenteritis and life-threatening
septicemia in immunocompromised individuals (3, 8).
Mortality from septicemia is quite high (>50%), and death may occur
within 1 to 2 days after the first signs of illness (8, 18).
A variety of endotoxins and exotoxins, including polysaccharide
capsules (16, 21, 23), a cytolytic hemolysin (15,
20), an elastolytic protease (10), and a phospholipase
A2 (19), have been implicated as virulence
factors for this organism. Among these, the cytolytic hemolysin, with a
molecular mass of 51 kDa, lyses erythrocytes (RBC) from various animals
by forming small pores in the cytoplasmic membrane and shows cytolytic
activity against cultured cell lines (15, 20). Our
laboratory demonstrated that this hemolysin caused vasodilation at a
far lower dosage than that required for cytotoxicity. This indicated
that hemolysin plays an important role in the pathogenesis of
hypotensive septic shock (9).
A 3.4-kb fragment of V. vulnificus DNA that encodes
hemolysin has been cloned, and its nucleotide sequence has been
determined (22). This DNA fragment contains two genes,
vvhB and vvhA, which are organized as a single
transcription unit termed the vvh operon. The
vvhA gene encodes the hemolysin, but the function of the
vvhB gene product is still unidentified. All V. vulnificus strains tested, regardless of source, carry the
vvhA gene for hemolysin production (20). A
possible binding site for cyclic AMP (cAMP) receptor protein (CRP) and
several sequences for the putative promoter of vvh were
suggested previously on the basis of homology to a consensus sequence
from Escherichia coli (22). However, regulation
of the vvh operon and environmental signals which stimulate its expression have not previously been characterized. In this report,
we have begun to elucidate the molecular mechanism by which the
bacterium modulates the expression of vvh genes by examining the nature of the glucose effect on the synthesis of the hemolysin. The
promoter activities of vvh in E. coli, deficient
in either adenylate cyclase or CRP, were analyzed by using a
vvh-luxCDABE transcriptional fusion. The effects of a
putative crp mutation and the addition of exogenous cAMP on
hemolysin production in V. vulnificus were also examined.
The bacterial strains and plasmids used in this study are listed in
Table 1. Hemolytic activities in culture
supernatant were determined by the method described by Shinoda et al.
(15), and a hemolytic unit was defined as the reciprocal of
the maximal dilution showing 50% hemolysis of human RBC (hRBC) or
sheep RBC (sRBC) solution (1%, vol/vol).
Effect of glucose on production of hemolysin in V. vulnificus.
To examine whether hemolysin production of
V. vulnificus C7184 is modulated by glucose, hemolytic
activities of cultures grown at 37°C in heart infusion (Difco,
Detroit, Mich.) broth supplemented with 2.0% NaCl were analyzed by
using hRBC at indicated time intervals (Fig.
1). Hemolytic activity appeared during
midexponential phase of growth and reached a maximum during stationary
phase. The addition of glucose at 0.5% to this culture resulted in
complete inhibition of hemolytic activity. In the presence of glucose,
the pH of the culture broth decreased, the cell yield was lower, and
the level of residual glucose remained at approximately 200 mg/ml
during stationary phase. The residual glucose levels in the culture
broth were determined with the Glucose Analyzer 2 (Beckman, Palo Alto, Calif.). In a previous report, our group showed that growth of V. vulnificus was highly pH dependent, with the highest growth rate
at pH 8.0 (11). It was possible that the decrease of
hemolytic activity of V. vulnificus cells with increasing
glucose was due to the decline of pH and/or reduced cell growth.
Therefore, 10 mM
N-tris(hydroxymethyl)methyl-2-aminoethanesulfonic acid (TES; Sigma, St. Louis, Mo.) buffering agent was added to the medium to
adjust pH, and then pH change, cell growth, and the level of residual
glucose were monitored (Fig. 1). When TES was added to the cells in the
presence of glucose, the pH and cell mass increased approximately to
the level observed in the nonglucose control culture and was
accompanied by a decrease of glucose in the culture broth. However, the
hemolytic activity was still completely inhibited and began to reappear
18 h later when the residual glucose in the culture broth was
depleted (Fig. 1B). It is apparent from these results that the
hemolytic activity is subject to repression by glucose in V. vulnificus and not regulation by growth phase or pH.
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FIG. 1.
Effect of glucose on growth and hemolysin activity of
V. vulnificus C7184. Cultures of V. vulnificus
were grown in heart infusion broth ( ,  ) or in heart infusion
broth supplemented with glucose alone ( ,  ) or with glucose and
TES together ( ,  ). Samples removed at the indicated times were
analyzed for growth and pH (A) and for hemolytic activity and residual
glucose (B). Filled symbols represent growth and hemolytic activity,
and open symbols represent pH and residual glucose changes in each
panel. Hemolytic activities were measured by using hRBC.
OD600, optical density at 600 nm.
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|
Construction of vvh-luxCDABE transcriptional fusion and
characterization of vvh promoter activity.
To
determine if the glucose-mediated repression is exerted at the
transcriptional level, we assessed the promoter activity of
vvh by constructing a vvh-lux fusion reporter.
Plasmid pYB9802 was constructed as outlined in the scheme in Fig.
2 by subcloning the regulatory elements
of the vvh operon from pYB9801 into pUCD615 (14)
carrying a promoterless luxCDABE operon. The parent plasmid, pYB9801, carries an EcoRI-HindIII fragment of
the vvh operon from pCVD702 (22) in pUC18. The
0.9-kb vvh DNA fragment was amplified by PCR using two
primers, SE-1 (5'-GACCATGATTACGCCAAGCTT-3') and SE-2
(5'-AAGAGAGGTAAACAGAGTCA-3'), which were located within the multicloning site of pUC18 and the open reading frame of
vvh, respectively.
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FIG. 2.
Construction of vvh-lux fusion plasmid
pYB9802. A PCR fragment carrying the regulatory region of the
vvh operon was subcloned into pUCD615 carrying promoterless
luxCDABE to create pYB9802. Filled blocks represent
lux DNA, open blocks represent vvh DNA, and thin
lines indicate the vector DNA used. Hybridizing locations of
oligonucleotide primers used for PCR are depicted by open arrows.
Abbreviations: B, BamHI; N, NdeI; P,
PstI; S, SmaI.
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|
E. coli CH1105, a MG1655 derivative known to contain
functional adenylate cyclase and CRP (
cya+
crp+) (
2), was transformed with pYB9802,
and cellular luminescence
of the culture was measured. Cellular
luminescence was measured
with a Lumat model 9501 luminometer
(Berthold, Berlin, Germany)
and was expressed in the
instrument's arbitrary relative light
units (RLU). Cultures were grown
at 30°C in Luria-Bertani broth
to an optical density at 600 nm of
1.0, and 1-ml samples from
each culture were taken and placed
into the cuvettes. The light
is produced by the products of the
luxCDABE genes controlled under
the
vvh
promoter; therefore, the luminescence level reflects the
promoter
activity of
vvh.
For the CH1105 strain containing pYB9802, luminescence activity
(defined as a wild-type level throughout this report) was
present at
1,100 RLU (Table
2). This level of
luminescence decreased
to about a 12-fold-lower level when the culture
was grown in the
presence of 0.5% glucose. This indicated that the
promoter activity
of
vvh in the
vvh-luxCDABE
fusion is repressed by glucose and
the glucose effect on the synthesis
of the hemolysin is exerted
at a transcriptional level in
E. coli. When cAMP was added at
5 mM to cells subjected to repression
by glucose, luminescence
was restored. This observation suggested that
the repression of
the
vvh promoter by glucose resulted from
the decrease of intracellular
cAMP and that the hemolysin synthesis may
be regulated by cAMP-controlled
catabolite repression.
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TABLE 2.
Luminescence in E. coli CH1105 and its
isogenic cya and crp mutants containing pYB9802
under various conditions
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|
Expression of vvh in E. coli with a
cya or crp background.
To further examine
the regulation of the vvh promoter in E. coli,
luminescence production levels from vvh-luxCDABE in E. coli CH1105 and in its isogenic mutants, which lack either
adenylate cyclase (cya) or CRP (crp), were
compared. When transformed with pYB9802, both cya mutant
CH1019 and crp mutant CH1133 cells expressed luminescence
levels below the detection limit of the luminometer used (Table 2).
Apparently, the promoter activity of vvh is completely repressed or very poorly expressed in the absence of active gene products of either cya or crp. Addition of cAMP
to the cya mutant containing pYB9802 restored luminescence,
and the level of luminescence was even higher than the wild-type level,
as will be discussed later (Table 2). In contrast to this, the
repressed luminescence in the crp mutant CH1133 cells was
not induced at all by addition of cAMP (Table 2). The luminescence in
CH1133 cells remained repressed regardless of the amount of cAMP added
(data not shown). These observations revealed that the cAMP exerts its
effects on the vvh promoter through CRP in E. coli.
Complementation of repression of vvhA in CH1133 with
E. coli CRP protein.
As a further test of this
hypothesis, we examined whether introduction of the crp gene
from E. coli could complement repression of the
vvh promoter of vvh-luxCDABE in CH1133 cells. For
this purpose, a 1.0-kb SspI-NruI fragment
carrying the crp gene of E. coli K-12 was
isolated from pHA7 (1) and was subcloned into the pACYC184
vector digested with PvuII. Since it has a p15A origin, the
resulting plasmid, pYB9803, is compatible with pYB9802 carrying oriS (oripSA) and pMBI (oripBR322)
origins. The crp mutant CH1133 containing pYB9802 was
transformed with pYB9803, and the CH1133 double transformant containing
both pYB9802 and pYB9803 was constructed. The luminescence in the
CH1133 double transformant was restored to a level comparable to the
wild-type level, whereas the repressed level of luminescence in the
cya mutant CH1019 containing pYB9802 was not restored at all
by transformation with pYB9803 (Table 2). Apparently, the E. coli
crp gene product introduced can recognize and activate the
vvh promoter, but the CRP is not functional for activation
of the vvh unless cAMP is provided. Combined with data described earlier, these findings led us to conclude that the promoter
of vvh of V. vulnificus is activated by the
cAMP-CRP complex.
Transformation with pYB9803 would provide CH1133 with multicopies of
crp, meaning that the number of CRP molecules in the
double
transformant cells could be relatively higher than that
in CH1105
cells, in which all CRP molecules are products of
crp carried on the chromosome. However, the level of luminescence
recovered
by the CH1133 double transformant was not significantly
higher than the
wild-type level. Only when exogenous cAMP was
added to this culture did
the level of luminescence increase,
with the highest level at 421,000 RLU (Table
2). The lack of
increased luminescence in cells carrying
extra copies of
crp can
be explained if intracellular levels
of cAMP are the limiting
factor rather than the number of CRP molecules
needed to form
a functional cAMP-CRP complex and activate the
vvh promoter on
vvh-luxCDABE. In agreement with
this assumption, addition of cAMP
to cells in which presumably a single
allele of
crp exists (such
as CH1105 or even CH1019)
increased the light production to a
level higher than the wild-type
level (Table
2).
Dependence of hemolysin production of V. vulnificus on
cAMP and cAMP receptor protein.
Results with E. coli
suggest that vvh is activated by the cAMP-CRP complex, but
it is not known if the same mechanism regulates expression of
vvh in V. vulnificus. To examine if the cAMP and CRP can regulate vvh in V. vulnificus, the
effects of adding cAMP or mutating crp on the production of
hemolysin were examined. Cultures of V. vulnificus MO6-24/O
were grown in heart infusion broth or heart infusion broth supplemented
with 0.5% glucose alone or with 0.5% glucose and cAMP together.
Hemolytic activities of samples removed at 12 h from each culture
were analyzed and compared. To ensure accurate sensitivity, sRBC were
employed to determine hemolytic activity in the supernatants of
cultures. The level of hemolytic activity suppressed in the presence of
glucose was recovered by the addition of cAMP (Fig.
3). When the amount of cAMP was increased
to 30 mM, the level of hemolytic activity reached higher levels than
that observed in the absence of glucose. This dose-dependent increase
of hemolytic activity brought about by cAMP indicates that the
intracellular level of cAMP is a limiting factor for hemolysin
synthesis in V. vulnificus.
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FIG. 3.
Dependency of hemolysin production of V. vulnificus on cAMP and CRP. (A) Cultures of strain MO6-24/O were
grown in heart infusion broth with various supplements added as
indicated. Samples removed at 12 h were analyzed for hemolytic
activity. Error bars represent standard errors of the mean. (B) Growth
and hemolytic activity of wild-type (, ) and crp
mutant CMM988 (, ) strains were compared. Samples removed at the
indicated times from cultures were analyzed for determination of growth
(filled symbols) and hemolytic activity (open symbols). For both
panels, sRBC were used for determination of hemolytic activities.
OD600, optical density at 600 nm.
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|
The dependence of hemolysin production of
V. vulnificus on
CRP was examined by isolating a spontaneous mutant of MO6-24/O
having a
crp phenotype. Isolation was carried out by methods
described
previously (
7), with only a slight modification.
Briefly, the
MO6-24/O strain was spread on selection medium containing
0.5%
galactose, 0.5% maltose, 1% tryptone, 0.5% yeast extract, 20 mM
Tris (pH 7.5), neutral red (30 µg/ml), 2.5% NaCl, and 1.5 mM
phosphomycin.
After overnight incubation, the mutants which showed gold
to pink
colony formation were transferred to selection medium
containing
10 mM cAMP to differentiate
cya mutants, and a
desired
crp mutant
was selected and referred to as CMM988.
The putative
crp mutation
of CMM988 was confirmed by testing
fermentation of carbon sources
on neutral red plates. The mutant
exhibited slow growth and no
fermentation of many sugars such as
maltose and
D-galactose, which
is consistent with the
phenotypes of a typical
crp mutant. When
the resulting
mutant was compared with its parental type, it appeared
to synthesize
much less hemolysin and the levels of hemolytic
activity were almost
undetectable (Fig.
3). Although other explanations
are possible, the
observation that hemolytic activity increased
by adding cAMP in a
dose-dependent fashion and decreased to undetectable
levels in the
putative
crp mutant indicates that the synthesis
of
hemolysin in
V. vulnificus is regulated by cAMP and
CRP.
Like other symbiotic and parasitic microorganisms,
V. vulnificus exists in two distinct habitats, seawater and the human
body.
Many differences such as the type and concentration of nutrients
are encountered when the organism is introduced into the human
body
from seawater environments. Among them, the increased level
of cAMP
could be one of the major stimuli that allows
V. vulnificus to recognize the new environment (inside the human body) and respond
by
producing
hemolysin.
cAMP-CRP plays a central role in carbon catabolite repression, by which
a rapidly metabolizable carbon source added to the
growth medium
represses the synthesis of many enzymes required
to metabolize other
carbon sources. This global regulatory system
has been well described,
especially for enteric bacteria (
4).
Besides regulation of
the synthesis of these catabolic enzymes,
cAMP-CRP catabolite
regulation has also been observed in the synthesis
of the toxin
proteins of several pathogenic bacteria. cAMP-CRP
has recently been
shown to activate hemolysin gene expression
in avian pathogenic
E. coli (
12). In contrast to this, CRP protein
negatively regulates the expression of cholera toxin and
toxin-coregulated
pilus genes in
Vibrio cholerae, a species
closely related to
V. vulnificus (
17). It has
also been reported that cAMP-CRP plays
a crucial role in the regulation
of virulence gene expression
and pathogenesis of
Salmonella
typhimurium (
6,
13). In this
report, we have shown that
the expression of the
V. vulnificus hemolysin gene is
dependent on cAMP and
crp gene function in both
E. coli and
V. vulnificus.
| |
ACKNOWLEDGMENTS |
We thank J. Oliver, J. G. Morris, Jr., and H. E. Choy for
providing the V. vulnificus C7184, V. vulnificus
MO6-24/O, and E. coli CH strains, respectively. We are also
indebted to J. G. Morris, Jr., C. I. Kado, and S. Y. Yoo
for providing the plasmids pCVD702, pUCD615, and pHA7, respectively.
This study was supported by a grant to S.H.C. and J.H.R. from the KRF
(GE-97-146), Republic of Korea.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Food Science and Technology, Institute of Biotechnology, Chonnam
National University, Kwang-Ju, 500-757, South Korea. Phone:
82-62-530-2146. Fax: 82-62-530-2149. E-mail:
shchoi{at}chonnam.chonnam.ac.kr.
| |
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Journal of Bacteriology, December 1999, p. 7639-7642, Vol. 181, No. 24
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Copyright © 1999, American Society for Microbiology. All rights reserved.
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