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Journal of Bacteriology, September 2000, p. 5009-5012, Vol. 182, No. 17
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Analysis of tnrA Alleles Which Result in
a Glucose-Resistant Sporulation Phenotype in Bacillus
subtilis
Byung-Sik
Shin,1
Soo-Keun
Choi,1
Issar
Smith,2 and
Seung-Hwan
Park3,*
Laboratory of Microbial and Bioprocess
Engineering1 and Genome Research
Center,3 Korea Research Institute of Bioscience
and Biotechnology, Yusong, Taejon, Korea 305-600, and
Department of Microbiology, Public Health Research
Institute, New York, New York 100162
Received 14 April 2000/Accepted 9 June 2000
 |
ABSTRACT |
Bacillus subtilis cells cannot sporulate in the
presence of catabolites such as glucose. During the analysis of
Tn10-generated mutants, we found that deletion of the
C-terminal region of the tnrA gene, which encodes a global
regulator that positively regulates a number of genes in response to
nitrogen limitation, results in a catabolite-resistant sporulation
phenotype. Analyses of nrg-lacZ and nasB-lacZ,
which are activated by TnrA under nitrogen limitation, showed that
C-terminally truncated TnrA activates nitrogen-regulated genes
constitutively. The relief of catabolite repression of sporulation may
result from the uncontrolled expression of the TnrA-regulated genes.
| |
TEXT |
Bacillus subtilis is a
gram-positive bacterium that can differentiate into heat-resistant
spores under conditions of nutrient deprivation. The initiation of
sporulation is controlled by phosphorylation of a single transcription
factor, Spo0A (reviewed in reference 9).
Accumulation of a high-enough concentration of Spo0A~P activates the
transcription of spoIIA, spoIIE, and
spoIIG, which are required for cell-type-specific gene
expression during the next stage of sporulation. The Spo0A
transcription factor is a member of a response regulator of a
two-component system, and there are at least three histidine kinases,
encoded by kinA, kinB, and kinC, that
are responsible for production of Spo0A~P. Normally, these kinases do
not transfer phosphate directly to Spo0A. Instead, Spo0F, a
single-domain response regulator, is phosphorylated by one of the
kinases and then transfers the phosphate to Spo0A by means of a
response regulator phosphotransferase, Spo0B. This extended version of
a two-component system may provide the multiple targets for regulation
by various environmental and physiological signals such as nutrient
depletion, cell density, and Krebs cycle, DNA synthesis, and DNA damage
(13).
It is known that the presence of catabolites such as glucose inhibits
sporulation. There are many mutations that lead to the catabolite-resistant sporulation (Crs) phenotype, such as those in
pai (12), hpr (24), and
rpoD (15). Some mutations in pts
(6), degS or degU (8, 16,
21), or gsiA (22) also yield the Crs
phenotype. Although the mechanisms underlying most Crs mutations are
still unknown, it seems that all known Crs phenotypes produce Spo0A~P
in the presence of glucose. Some mutations in spo0A, such as
rvtA11 and sof-1, that bypass the phosphorelay also show the Crs phenotype, indicating that phosphorelay may be a main
target for catabolite repression of sporulation in the wild type
(10, 14, 27, 28).
In this paper, we show that deletion of the C-terminal region of TnrA
also results in the Crs phenotype. TnrA is a regulatory protein that is
involved in the activation of nitrogen-regulated genes, such as
gabP (
-aminobutyrate permease), nasB (nitrate assimilatory enzymes), ure (urease), and nrgA
(putative ammonium permease), during nitrogen-limited growth (4,
31). Our findings suggest that deletion of the C-terminal region
of TnrA resulted in constitutive expression of the nitrogen-regulated
genes and that this uncontrolled expression of TnrA-regulated genes
results in cells with a Crs phenotype that can sporulate in the
presence of a normally inhibitory concentration of glucose.
Isolation of the tnrA::Tn10
mutant.
During the screening of Crs mutants generated by
mini-Tn10 mutagenesis of the IS75 strain, we found that a
tnrA allele, in which Tn10 integrated into an
open reading frame (ORF) of the tnrA gene, showed the
glucose-resistant sporulation phenotype. The
tnrA::Tn10 mutant efficiently
sporulates in DSM (Difco sporulation medium) containing 2% glucose
(DSMG), showing about 50% sporulation frequency. The sporulation
frequency is decreased to about 10% in DSM supplemented with both 2%
glucose and 0.2% glutamine (DSMGQ), indicating that catabolite
repression of sporulation is only partially overcome in the presence of
both glucose and glutamine. The Crs phenotype resulting from the
tnrA::Tn10 allele is not a
strain-specific property. We produced the
tnrA::Tn10 mutation in two other
strains, 168 and JH642, and found that these strains also showed
similar sporulation phenotypes (see Table 1 for JH642). We used the
JH642 strain for further genetic study.
To establish a true tnrA-null genotype, we constructed a
deletion-insertion mutation where the internal tnrA ORF was
replaced with an erm gene cassette, creating strain BS9909
(See Fig. 2). Interestingly, this null allele of the tnrA
gene resulted in a glucose-sensitive sporulation phenotype, which is
similar to that of the wild-type strain JH642 (Table
1). This fact indicated that the Crs
phenotype is not caused by the tnrA null mutation. Wray et
al. also reported that the
tnrA62::Tn917 mutation did not relieve
glucose repression of sporulation in nutrient sporulation medium
containing 1% glucose (32). We observed that insertion of
Tn10 within the C-terminal region of the tnrA ORF
created a chimeric protein in which seven codons of the C-terminal
tnrA ORF were replaced with 11 codons provided by the
Tn10 sequence (Fig. 1). This
suggests that the Crs phenotype resulting from the
tnrA::Tn10 mutation is due to chimeric
TnrA protein.
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FIG. 1.
Map of the chromosomal region of tnrA. The
arrows indicate the coding regions of the genes. The location of the
Tn10 transposon insertion is indicated. C-terminal regions
of both the TnrA wild type and the TnrA chimera encoded by
tnrA::Tn10 are also shown. Amino acids
translated by the Tn10 sequence are underlined.
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Construction of C-terminally deleted tnrA mutants.
Since it seemed that truncation of the C-terminal region of
tnrA may be important for the Crs phenotype that we
observed, a set of deletion mutations was made in which C-terminal
amino acid residues of the tnrA product were serially
removed (Fig. 2). All of these constructs
were integrated into the original tnrA locus along with the
erm gene cassette. Construction of the mutations was
confirmed by both Southern hybridization and sequencing of DNA
fragments obtained by PCR. As shown in Table 1, strains BS9913 and
BS9932, harboring 
tnrA7 (seven C-terminal amino acids deleted) and tnrA20 (20 C-terminal amino acids deleted),
respectively, showed Crs phenotypes similar to that of the
tnrA::Tn10 mutant, though the BS9913
strain had decreased sporulation frequencies in both DSM and DSMG
compared to that of BS9932. Strain BS9914 containing
tnrA34 (34 C-terminal amino acids deleted) exhibited a
glucose-sensitive sporulation phenotype as well. The strain that
contains the intact tnrA gene with an erm
cassette showed a sporulation phenotype similar to that of strain JH642
(data not shown).
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FIG. 2.
Construction of tnrA mutations. The DNA
fragments used to construct the tnrA mutations and the
erythromycin resistance gene are diagrammed. The flanking DNA fragments
used for chromosomal integration of tnrA mutations are not
shown. The 1.1-kb erm cassette is not drawn to scale. Arrows
indicate the coding regions of the genes. C-terminally deleted
tnrA mutations were constructed by insertion of stop codons
at desired sites in the tnrA ORF. aa, amino acids.
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The Crs-type
tnrA mutants (BS9913 and BS9932) grew more
slowly than did wild-type cells in DSM (generation time of 27 min
versus 20 min for JH642) and had a reduced cell yield (final optical
density at 600 nm of 1.9 to 2.1 versus 2.4 to 2.6 for JH642).
There was
no significant difference in the growth rates of the
tnrA-null mutant (BS9909) and the wild-type strain in
DSM.
The sporulation phenotypes of strains with the
tnrA alleles
were somewhat variable and seemed to be sensitive to specific
growth
conditions. To analyze sporulation phenotypes of the
tnrA mutants more quantitatively, expression of a
spoIIA-lacZ
fusion
in various
tnrA mutants were examined. Since
expression of
spoIIA reflects production of Spo0A~P, one
of the key transcription factors
in sporulation initiation, monitoring
-galactosidase activity
from a
spoIIA-lacZ strain
provides a good indication of the ability
of cells to initiate
sporulation. As shown in Table
1, expression
levels of the
spoIIA-lacZ fusions in the wild-type strain (JH642),
the
tnrA-null mutant (BS9909), and the strain having
tnrA7 (BS9914)
were repressed by 2% glucose, but strains
having
tnrA7 (BS9913)
and
tnrA20 (BS9932)
expressed
spoIIA-lacZ during growth in DSMG.
These results
agree with previous data on sporulation frequency.
Interestingly,
spoIIA-lacZ expression in the
tnrA7 and
tnrA20 mutants was barely repressed in DSMGQ culture,
although sporulation
frequencies were reduced in the same medium. This
fact suggests
that, in DSMGQ culture, Crs mutants can produce enough
Spo0A~P
for activation of
spoIIA but the sporulation
process is still
repressed. In summary, it is likely that the Crs
phenotype exhibited
in DSMG by strains with the truncated
tnrA alleles was mainly
due to a loss of C-terminal amino
acid residues from
TnrA.
Analysis of nitrogen regulation of tnrA mutants.
TnrA is a global regulator that positively regulates a number of genes
and operons in response to nitrogen limitation. Since the Crs phenotype
is apparently caused by truncated TnrA protein, we checked strains with
the different tnrA alleles to determine whether their
nitrogen-regulating function was normal. Transcriptional lacZ fusions to nrg and nasB, which
are activated by TnrA under nitrogen-limited conditions, were
constructed in various tnrA mutants, and -galactosidase
activities were monitored during growth in TSS minimal medium. We used
0.2% glutamate as a limiting nitrogen source and 0.2% glutamate plus
0.2% (wt/vol) glutamine as an excess nitrogen source. As previously
reported (31), TnrA was responsible for most of the
induction of the nrg-lacZ and nasB-lacZ
expression during nitrogen-limited growth. While the expression of
fusions in the wild-type strain (JH642) was strongly induced during
nitrogen-limited growth, induction was barely observed in the strains
BS9909 and BS9914 (Table 2).
Interestingly, in the strains showing the Crs phenotype (BS9913 and
BS9932), the nrg-lacZ and nasB-lacZ expression
levels were increased in both nitrogen-limited and excess-nitrogen
conditions. This fact suggests that TnrA7 and TnrA20
constitutively activate nitrogen-regulated genes, such as
nrg and nasB, irrespective of nitrogen
availability.
Although the metabolic signal molecule that regulates TnrA activity is
not known, it is generally believed that glutamine
synthetase (GS) is
required for production and/or transduction
of the nitrogen signal
(
31). If the Crs phenotypes exhibited
by strains with the
tnrA7 and
tnrA20 alleles are caused by
constitutive
activation of nitrogen-regulated genes, then the
glnA mutant,
which cannot synthesize GS, should also have
the Crs phenotype,
because nitrogen-regulated genes are activated
constitutively
in the
glnA mutant (Table
2) (
31).
However, as the
glnA mutant
is a glutamine auxotroph, we
could not examine the sporulation
phenotype in DSMG. Instead,
expression of
spoIIA-lacZ was measured,
since the
tnrA7 and
tnrA20 mutants expressed
spoIIA-lacZ during
growth in DSMGQ culture even when
sporulation was partially repressed.
As shown in Table
1, sporulation
frequency of the
glnA mutant
was partially repressed in the
DSMGQ culture, but expression of
spoIIA-lacZ was induced,
similar to the results obtained for the
tnrA7 and
tnrA20 mutants. Furthermore, we also observed that
spoIIA-lacZ expression of the
glnA mutant grown
in DSMGQ was almost
repressed again by mutational inactivation of the
tnrA gene (Table
1), indicating that
spoIIA-lacZ
expression of the
glnA mutant
resulted from constitutive
expression of the nitrogen-regulated
genes. All of the results we
obtained imply that constitutive
expression of nitrogen-regulated genes
caused by C-terminally
truncated TnrA results in derepression of
sporulation in DSMG
culture.
It is difficult to explain why the constitutive expression of
tnrA-regulated genes results in a Crs phenotype in DSMG.
Recently,
it was reported that, in the histidine utilization
(
hut) operon,
carbon catabolite repression (CCR) was
partially relieved in the
glnA mutant (
33). Since
this partial relief of CCR was suppressed
by
tnrA mutation,
it was proposed that the defect in CCR of the
hut operon
seen in the
glnA mutant could result from the inappropriate
expression of TnrA-regulated genes. The observation that the
nrg-lacZ and
nasB-lacZ fusions are also expressed
constitutively in the
Crs-type
tnrA mutants raises the
possibility that both the Crs
phenotype of the
tnrA mutants
and the relief of CCR of the
hut operon may result from the
same metabolic imbalance caused by
the uncontrolled activation of
TnrA-regulated genes. It is also
possible that the intracellular
concentration of GTP (and/or GDP),
which is closely related to
induction of sporulation (
17,
18),
could be affected by
inappropriate expression of TnrA-regulated
genes. We observed that the
upstream region of a putative xanthine-uracil
permease gene
(
yunJ) has two TnrA-binding consensus sequences
(TGTNAN
7TNACA), which are upstream DNA sequences commonly
found
in TnrA-regulated genes (
31).
yunJ is
followed by three genes,
yunK,
yunL, and
yunM, which may be organized in an operon structure.
Since
yunL also codes for a uricase-like protein, the gene of
this
operon may code for a system to take up and degrade purine.
As xanthine
dehydrogenase activity is also subject to the GS-dependent
signaling
pathway (
3), C-terminally truncated TnrA can stimulate
constitutive degradation of purine molecules, resulting in a decrease
in the GTP pool and induction of sporulation initiation. Examination
of
the intracellular GTP pool in the Crs-type
tnrA mutant
should
help to determine the accuracy of this
hypothesis.
It is interesting to note that
spoIIA-lacZ expression in the
BS9909 and BS0002 strains resulted in about a twofold-higher
level of
-galactosidase activity than that of the wild-type control.
This
observation suggests that TnrA protein negatively affects
formation of
Spo0A~P. Recently, Wang et al. (
30) discovered
an operon
that encodes a KipI protein that specifically inhibits
the
autophosphorylation reaction of KinA. Interestingly, TnrA
is required
for activation of an operon containing a
kipI gene.
Wang et
al. showed that, in the absence of functional TnrA, KipR,
a product of
another gene of the
kipI-containing operon, completely
represses the expression of the
kipI-containing operon. We
do
not know what exactly is responsible for stimulation of
spoIIA-lacZ by the
tnrA null mutation, but
because KipI is a potent inhibitor
of KinA activity, loss of activation
of the
kip operon, which
may be caused by the
tnrA null mutation, should stimulate formation
of Spo0A~P.
Strain BS9914 also has a higher level of
spoIIA-lacZ expression in DSM than does wild type, but expression was strongly
repressed in DSMG and DSMGQ medium. Thus, it seems that
tnrA34 is not a null allele, though the phenotypes of
sporulation frequency
and nitrogen regulation are very similar to those
of the null
mutant. We do not know the exact reason for strong
repression
of the
spoIIA-lacZ expression of strain BS9914 in
DSMG and
DSMGQ.
TnrA protein belongs to the MerR family of regulators (
29).
These MerR-type proteins are characterized by an N-terminal
DNA-binding
domain which is highly homologous within the group
and which shares
homology with various C-terminal domains specific
to general substrates
such as mercuric ions (MerR [
20]), thiostrepton
(TipA
[
11]), or oxidative stress (SoxR
[
1]). Although the
effector molecule of TnrA is still
unknown, the results of analysis
of the
tnrA mutants
presented here suggest that the C-terminal
region of the TnrA protein
participates in sensing the hypothetical
inducer molecule. As the
deletion of the C-terminal region of
TnrA allows activation of target
genes without the inducer molecule,
it seems that separation of the
DNA-binding domain from the C-terminal
region mimics activation of TnrA
naturally occurring under nitrogen-limited
conditions. Recently,
Baranova et al. reported that the activity
of Mta, a MerR-type
regulator involved in the regulation of multidrug
transporters, is also
stimulated by removal of a C-terminal inducer-binding
domain
(
2). Thus, it seems likely that the activity of the
DNA-binding domain (possibly having an affinity for the target
promoter) is inhibited by the C-terminal domain under repressed
conditions and that this inhibition is relieved by the interaction
of
an inducer molecule with the C-terminal domain under derepressed
conditions. This may be a common mechanism for regulation of MerR-type
proteins.
| |
ACKNOWLEDGMENTS |
We thank P. Stragier for providing plasmid pDG1728 and S. Fisher
for providing plasmid pGLN14 and for valuable comments on the
manuscript. We are grateful to J.-G. Pan and J.-K. Lee for useful discussions and suggestions on the manuscript. We also thank Y.-K. Park for providing technical assistance.
This work was supported in part by grant HS2540 from the Ministry of
Science and Technology of Korea.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Genome Research
Center, Korea Research Institute of Bioscience and Biotechnology, P.O. Box 115, Yusong, Taejon, Korea 305-600. Phone: 82-42-860-4412. Fax:
82-42-860-4594. E-mail: shpark{at}mail.kribb.re.kr.
| |
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Journal of Bacteriology, September 2000, p. 5009-5012, Vol. 182, No. 17
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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