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Journal of Bacteriology, August 2001, p. 4648-4651, Vol. 183, No. 15
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.15.4648-4651.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Involvement of Stringent Factor RelA in Expression
of the Alkaline Protease Gene aprE in Bacillus
subtilis
Michihiro
Hata,
Mitsuo
Ogura, and
Teruo
Tanaka*
Department of Marine Science, School of
Marine Science and Technology, University of Tokai, Shimizu,
Shizuoka 424-8610, Japan
Received 16 April 2001/Accepted 19 April 2001
 |
ABSTRACT |
Expression of Bacillus subtilis aprE, encoding an
extracellular alkaline protease, is positively regulated by
phosphorylated DegU, the regulator of a two-component regulatory
system, DegS-DegU. We found that the expression of an
aprE'-'lacZ fusion was greatly reduced in a disruption
mutant with a mutation of relA, which encodes the stringent
factor RelA. The level of DegU in the relA mutant was
similar to that in the wild-type cell. A relA degU double
mutation did not result in a further decrease of the
aprE'-'lacZ level found in a degU single
mutant. The expression of the aprE'-'lacZ fusion in the
relA mutant was stimulated by multicopy degR or the degU32(Hy) and degS200(Hy) mutations that
cause the stabilization of phosphorylated DegU. Furthermore, the
expression of sacB'-'lacZ, which is also dependent on
phosphorylated DegU, was stimulated by the relA mutation,
and this stimulation was not seen in the relA degU double
mutant. These results show that RelA (or its product
guanosine-3',5'-bisdiphosphate [pp Gpp]) does not affect the
phosphorylation of DegU and suggest that it participates in the
expression of aprE and sacB through the
regulation of DegU-dependent transcription.
| |
TEXT |
Bacillus subtilis
produces two major extracellular proteases, the alkaline and neutral
proteases, which are produced after the cessation of exponential
growth. The expression of the aprE gene, encoding the
alkaline protease, is regulated at the level of transcription both by
positive regulators including the two-component regulatory system
DegS-DegU and by negative regulatory factors (5, 7, 12,
20). Among the positive factors, the DegS-DegU pair plays a
central role, since disruption of either degS or degU results in a substantial decrease in aprE
expression (3, 14), and obliterates the effects of the
positive regulators (11, 15, 17, 18).
Microorganisms living in nature adapt to changing environments such as
starvation, desiccation, osmotic stress, and temperature variations for
survival. One such example of adaptation is the stringent response in
which the synthesis of many high-molecular-weight components including
stable RNA (rRNA and tRNA) becomes limited while gene expression of
some others including biosynthesis genes of amino acids is activated
(1). This response leads to adjustments of gene expression
which are thought to be mediated by guanosine 3',5'-bisdiphosphate
(ppGpp) synthesized by the stringent factor RelA (1).
ppGpp accumulation is provoked by many stress conditions including heat
shock, oxidative stress, and deficiency of amino acids and carbon,
nitrogen, and phosphate sources. Numerous studies have been performed
on the Escherichia coli and Salmonella enterica serovar Typhimurium stringent response (1), and recently
the Bacillus subtilis relA gene was cloned and studied by
Wendrich and Marahiel (23).
B. subtilis is a gram-positive bacterium living in soil,
where it may encounter severe fluctuations in the environment,
including deficiency of nutrients and a variety of stresses. It may
therefore be reasonable to assume that a number of adaptive responses
have evolved to cope with such situations. One such example will be the
secretion of proteases: they may be secreted from B. subtilis cells in response to limitation of the intracellular
nitrogen source so that they can digest high-molecular-weight proteins present in the environments and provide the cells with amino acids. Since these enzymes are produced in considerable amounts, the production may be strictly controlled in response to the environmental conditions. These considerations prompted us to examine whether the
stringent response is involved in aprE expression. In this paper we show that RelA exerts positive and negative regulation on
aprE and sacB, respectively, in a DegU-dependent manner.
Involvement of relA in aprE
expression.
The relA gene, encoding a 734-amino-acid
protein, is located at a region from nucleotides 2821998 to 2819794 on
the B. subtilis chromosome (8). We disrupted
the relA gene in strain YY102 (see the legend to Fig. 1) by
insertion of tetracycline resistance gene (tet)
(6) at the EcoT22I site (codon 333) by a
double-crossover event. As shown in Fig.
1, the expression of
aprE'-'lacZ was greatly reduced in the resultant
relA333 mutant (HT1013) grown in Schaeffer medium.
Disruption of the downstream gene yrvI (8) did
not affect aprE'-'lacZ expression (data not shown),
indicating that the above result was not due to a polar effect of
relA disruption on the downstream gene. The level of ppGpp
in strain HT1013 during vegetative and stationary-phase growth in
Schaeffer medium was found to be about 1/20 the level found in the
wild-type strain, CU741 (data not shown).
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FIG. 1.
Effect of disruption of relA on
aprE'-'lacZ expression. Cells grown overnight in
Luria-Bertani medium were inoculated into Schaeffer sporulation medium
(19) and harvested at hourly intervals after the cessation
of logarithmic growth.  -Galactosidase activities are shown in Miller
units. Numbers on the x axis represent the growth time in
hours relative to the end of vegetative growth (T0). Symbols:  ,
YY102 relA+,  , HT1013 relA333.
Strain YY102 (leuC7 trpC2 aprE::pSKK25) was constructed
by insertion of a pUC18-derived, kanamycin resistance plasmid, pSKK25,
carrying aprE'-'lacZ at the aprE locus of CU741
(22) by Campbell-type recombination. Strain HT1013 is
described in the text.
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It has been demonstrated that the total level of
aprE
expression is the sum of
degS-degU-dependent and
-independent expression
and that the former pathway accounts for most
of the
aprE'-'lacZ expression in nutritional medium
(
14). We next examined which
of the two pathways leading
to
aprE expression described above
is subject to RelA
regulation. We constructed two strains carrying
deletions in either
degU or both
degU and
relA so that we
could
examine the effect of the
relA333 mutation on
DegU-independent
aprE expression. As shown in Fig.
2, the
-galactosidase activities
found
in the two strains were almost the same. These results show
that
DegU-dependent
aprE expression but not DegU-independent
expression
is subject to control by RelA.
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FIG. 2.
Effect of relA mutation on
aprE'-'lacZ expression in a degU-deficient
mutant. The experimental conditions were the same as those described in
the legend to Fig. 1. Numbers on the x axis represent the
growth time in hours relative to the end of vegetative growth (T0).
Colonies formed on a plate were inoculated into Luria-Bertani medium
containing appropriate antibiotics (5 µg of chloramphenicol per ml
and 10 µg of tetracycline per ml) and incubated overnight at 37°C.
A 2-ml volume of the overnight culture was inoculated in 50 ml of
Schaeffer sporulation medium without antibiotics, and samples were
withdrawn at the times indicated. The data shown are those obtained in
one of two sets of experiments performed under the same conditions and
at the same time. -Galactosidase activities are shown in Miller
units. The parental strain B. subtilis CU741 did not show
detectable -galactosidase activity during the growth period.
Symbols: , HT2113 (relA333 degU);  , YY309
(degU). Strain HT2113 (leuC7 trpC2 relA333
degU::cat aprE::pSKK25) was constructed
by transformation of HT1013 with DNA from TT711 (leuC7 trpC2
degU::cat) (20). Strain YY309
(leuC7 trpC2 degU::cat
aprE::pSKK25) was constructed by transformation of YY102 with
DNA from TT711.
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Effect of relA mutation on degU
expression.
If the relA disruption caused a reduction
in degU expression, the decrease in the expression of
aprE in the relA-deficient mutant could be
ascribed to a reduced level of DegU. To test this possibility, we
examined the expression of degU by Western analysis of the
relA strain. As shown in Fig.
3, the levels of DegU protein were
similar in strain HT1013 and the wild-type strain throughout the time
examined. We note that the highest level of DegU was attained after
around T1 to T2, which is in contrast to the gradual decline of
-galactosidase activities derived from the degU'-'lacZ fusion after T0 (reference 17 and data not shown). These
results indicate that the -galactosidase activities derived from the degU'-'lacZ fusion do not reflect the actual level of DegU
protein in the cell. This may be due either to the degradation of the chimeric -galactosidase composed of the N-terminal DegU and E. coli -galactosidase or to the instability of mRNA carrying the mRNA for the fusion protein.
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FIG. 3.
Effect of relA disruption on degU
expression as determined by Western analysis of DegU. B. subtilis HT1227 (leuC7 trpC2 relA333) was constructed
by transformation of YY102 with DNA from HT1013. Numbers above the
photograph indicate the growth time in hours relative to T0. DegU was
purified by a previously described method (14), and the
antibody against DegU was commercially prepared by Sawady Co. For
Western blot analysis, cells collected from 10-ml cultures were
resuspended in 1 ml of TE buffer (10 mM Tris-HCl [pH 8.0], 1 mM EDTA)
containing 1 mM phenylmethylsufonyl fluoride, and disrupted in a French
press. Proteins were separated by electrophoresis in a 12.5%
polyacrylamide gel, and DegU bands were detected by the DegU antibody
using the BM Chemiluminescence Western blotting kit (Boehringer
Mannheim Co.).
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Enhanced expression of aprE by multicopy degR,
degU32(Hy), and degS200(Hy) mutations in a
relA background.
It has been demonstrated that
multicopy degR or the degS200(Hy) mutation causes
the stabilization of phosphorylated DegU (4, 5, 21).
Similarly, the DegU protein encoded by the degU32(Hy) gene
retains phosphate longer than the wild-type DegU protein does
(4). The presence of these genetic traits results in
enhanced expression of aprE'-'lacZ. Therefore, if the
reduced expression of aprE'-'lacZ by the relA
mutation is due to a defect in the phosphorylation process of DegU, the
enhancing effects would not be observed in the relA
background. In fact, the stimulatory effects of multicopy
degR and the degU32(Hy) mutation, which require
phosphorylation of DegU, are not observed in degS-deficient
mutants (5, 15). A multicopy plasmid, pNC61, that we used
for this experiment carries degR in a vector, pNC6
(15, 16). We found that the expression of
aprE'-'lacZ in the relA cell (17% of the control
level) was increased about 250-fold by the presence of pNC61 under
conditions where the multicopy degR effect in the
relA+ cell was 96-fold (Table
1, experiment 1). Likewise, both the degU32(Hy) and degS200(Hy) mutations caused the
stimulation of aprE'-'lacZ expression in the relA
cells to levels similar to those attained in the
relA+ cells (Table 1, experiment 2). The
differences in the magnitude of enhancement between multicopy
degR and the degU32(Hy) or degS200(Hy) mutations may be due to the different modes of stabilization of phosphorylated DegU, although the precise mechanisms of stabilization by these genetic traits remain to be studied. These results show either
that DegU is phosphorylated in part in the relA cell and stabilized by multicopy degR or the degU32(Hy)
and degS200(Hy) mutations or that it is phosphorylated to a
level similar to the wild-type level but does not show full activity
due to a defect in some other process in the pathway of aprE
expression.
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TABLE 1.
Expression of aprE'-'lacZ in B. subtilis strains carrying either multicopy degR or
degU32(Hy) and degS200(Hy) mutations
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Effect of relA mutation on sacB'-'lacZ
expression.
The expression of the sacB gene, encoding
extracellular levansucrase, is also positively regulated by
phosphorylated DegU. This was shown by the effect of a defect in
levansucrase production by a strain carrying the degS42
mutation, which results in the production of an
autophosphorylation-defective DegS protein, and by overproduction of
the enzyme by strains carrying the degU32(Hy) or
degS200(Hy) mutation or multicopy degR (10,
16). We therefore examined the effect of relA
deficiency on sacB expression by using a
sacB'-'lacZ translational fusion (9). In
contrast to its negative effect on aprE expression, the
relA mutation caused an enhancement of
sacB'-'lacZ expression (Fig.
4). To test whether the enhanced
expression of sacB in the relA-deficient mutant
is still dependent on DegU, we introduced a degU null
mutation into the relA mutant. As shown in Fig. 4, a
degU deletion abolished the enhanced expression of
sacB'-'lacZ caused by the relA mutation, and the
resultant level was as low as that seen in the
relA+ degU strain, indicating that
the enhanced expression of sacB'-'lacZ in the
relA mutant requires DegU.
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FIG. 4.
Effect of relA and degU
disruptions on sacB'-'lacZ expression. Cells were grown in
SCHE medium (9) containing 2% sucrose, collected at the
indicated times, and determined for -galactosidase activity. Numbers
on the x axis represent the growth time in hours relative to
the end of vegetative growth (T0). The data shown are those obtained in
one of two sets of experiments performed under the same conditions and
at the same time. The host strain, B. subtilis CU741, did
not show detectable -Galactosidase activity during the growth
period. -Galactosidase activities are shown in Miller units.
Symbols: , IN6052 (relA+); , IN7461
(relA333); , IN6711 (relA+
degU);  ; IN7141 (relA333 degU). Strain IN6052
[leuC7 trpC2 amyE::(sacB'-'lacZ erm)] was
constructed by transformation of CU741 with DNA from QB4624
(9). Strain IN7461 [leuC7 trpC2
relA::tet amyE::(sacB'-'lacZ erm)]
was constructed by transformation of HT1227 with DNA from QB4624.
Strains IN6711 and IN7141 were constructed by transformation of IN6052
and IN7461, respectively, with DNA from TT711.
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In this work, we constructed a
relA333 disruption mutation
and found that it exerts different effects on the expression of
the
aprE and
sacB genes, although they are in the
same DegU regulon
(
13). From the findings that
relA deficiency caused a reduction
in
aprE'-'lacZ
expression but did not affect the intracellular
level of DegU protein
(Fig.
2), two possibilities are conceivable
concerning the target site
of RelA (or its reaction product ppGpp)
in
aprE expression.
One is that the target is in a pathway leading
to the phosphorylation
of DegU. This possibility is, however,
unlikely because of the
following two results. First, the expression
of
aprE'-'lacZ
was stimulated by multicopy
degR or the
degU32(Hy)
and
degS200(Hy) mutations in the
relA cell (Table
1). Since the
stimulation of
aprE expression by these genetic traits is dependent
on
phosphorylated DegU (
5,
15,
21), the results indicate
that
DegU is phosphorylated at least in part in the
relA cells.
Second, the expression of both the
aprE and
sacB
genes is known
to be regulated positively by phosphorylated DegU
(
4,
10,
21), but the effects of the
relA
mutation on these genes were
found to be opposite (Fig.
1 and
4). The
other possible target
site may be in the transcription process, since
it is generally
accepted that ppGpp affects transcription through
interaction
with RNA polymerase (references
1 and
2 and
references therein).
When this notion is applied to the results
obtained in this study,
it follows that the phosphorylated
DegU-dependent transcription
is enhanced or inhibited by ppGpp for
aprE and
sacB, respectively.
Here, phosphorylated
DegU plays a major role, since a disruption
of
degU in a
relA333 mutant resulted in complete inhibition of
the
expression of both genes (Fig.
2 and
4). It should be noted
that ppGpp
regulates numerous genes in positive and negative ways
(
1).
An entirely different notion is also possible, i.e., that there are two
targets of RelA in the process of
aprE or
sacB
expression.
For
sacB expression, for example, one target
reduces phosphorylation
of DegU while the other enhances some other
process, with an overall
effect being positive in the expression of
sacB. This possibility,
however, may be excluded, since if
it were true, a
degU knockout
would affect only the DegU
pathway and would not result in the
complete loss of
sacB'-'lacZ activity shown in Fig.
4. Therefore,
we favor
the hypothesis that RelA affects
aprE and
sacB
expression
at the level of
transcription.
The differential regulation of
aprE and
sacB
expression reported in this study is reminiscent of the opposite effect
of high
salt concentrations on
aprE and
sacB
expression reported by Kunst
and Rapoport (
9). Although
this seemed to imply a common mechanism
between
relA
deficiency and high salt concentrations, addition
of 1 M NaCl
stimulated
sacB'-'lacZ expression in both
relA+ and
relA strains, indicating
that the high-salt effect is not
mediated through RelA (data not
shown).
| |
ACKNOWLEDGMENTS |
We thank F. Ikebuchi, K. Nakata, and H. Ishida for technical
assistance; Y. Sadaie for a bacterial strain; and M. Itaya for a
plasmid. We also thank K. Ochi, Y. Ohashi, and N. Saito for ppGpp measurement.
This work was supported in part by a grant-in-aid for scientific
research from the Ministry of Education, Science and Culture of Japan
and by RIKEN Biodesign Research.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Marine Science, School of Marine Science and Technology, Tokai
University, Shimizu, Shizuoka 424-8610, Japan. Phone: (543) 34-0411. Fax: (543) 34-9834. E-mail:
teruot{at}scc.u-tokai.ac.jp.
| |
REFERENCES |
| 1.
|
Cashel, M.,
D. R. Gentry,
V. J. Hernandez, and D. Vinella.
1996.
The stringent response, p. 1458-1496.
In
F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella; cellular and molecular biology, 2nd ed. American Society for Microbiology, Washington, D.C.
|
| 2.
|
Choy, H. E.
2000.
The study of guanosine 5'-diphosphate 3'diphosphate-mediated transcription regulation in vitro using a coupled transcription-translation system.
J. Biol. Chem.
275:6783-6789[Abstract/Free Full Text].
|
| 3.
|
Dahl, M. K.,
T. Msadek,
F. Kunst, and G. Rapoport.
1991.
Mutational analysis of the Bacillus subtilis DegU regulator and its phosphorylation by the DegS protein kinase.
J. Bacteriol.
173:2539-2547[Abstract/Free Full Text].
|
| 4.
|
Dahl, M. K.,
T. Msadek,
F. Kunst, and G. Rapoport.
1992.
The phosphorylation state of the DegU response regulator acts as a molecular switch allowing either degradative enzyme synthesis or expression of genetic competence in Bacillus subtilis.
J. Biol. Chem.
267:14509-14514[Abstract/Free Full Text].
|
| 5.
|
Henner, D. J.,
E. Ferrari,
M. Perego, and J. A. Hoch.
1988.
Localization of Bacillus subtilis sacU(Hy) mutations to two linked genes with similarities to the conserved procaryotic family of two-component signaling systems.
J. Bacteriol.
170:5102-5109[Abstract/Free Full Text].
|
| 6.
|
Itaya, M.
1992.
Construction of a novel tetracycline resistance gene cassette useful as a marker on the Bacillus subtilis chromosome.
Biosci. Biotechnol. Biochem.
56:685-686[Medline].
|
| 7.
|
Kunst, F.,
M. Debarbouille,
T. Msadek,
M. Young,
C. Mauel,
D. Karamata,
A. Klier,
G. Rapoport, and R. Dedonder.
1988.
Deduced polypeptides encoded by the Bacillus subtilis sacU locus share homology with two-component sensor-regulator systems.
J. Bacteriol.
170:5093-5101[Abstract/Free Full Text].
|
| 8.
|
Kunst, F.,
N. Ogasawara,
I. Moszer,
A. M. Albertini,
G. Alloni,
V. Azevedo,
M. G. Bertero,
P. Bessieres,
A. Bolotin,
S. Borchert,
R. Borriss,
L. Boursier,
A. Brans,
M. Braun,
S. C. Brignell,
S. Bron,
S. Brouillet,
C. V. Bruschi,
B. Caldwell,
V. Capuano,
N. M. Carter,
S. K. Choi,
J. J. Codani,
I. F. Connerton,
A. Danchin, et al.
1997.
The complete genome sequence of the gram-positive bacterium Bacillus subtilis.
Nature
390:249-563[CrossRef][Medline].
|
| 9.
|
Kunst, F., and G. Rapoport.
1995.
Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis.
J. Bacteriol.
177:2403-2407[Abstract/Free Full Text].
|
| 10.
|
Lepesant, J.-A.,
F. Kunst,
J. Lepesant-Kejzlarova, and R. Dedonder.
1972.
Chromosomal location of mutations affecting sucrose metabolism in Bacillus subtilis.
Mol. Gen. Genet.
118:135-160[Medline].
|
| 11.
|
Msadek, T.,
F. Kunst,
A. Klier, and G. Rapoport.
1991.
DegS-DegU and ComP-ComA modulator-effector pairs control expression of the Bacillus subtilis pleiotropic regulatory gene degQ.
J. Bacteriol.
173:2366-2377[Abstract/Free Full Text].
|
| 12.
|
Msadek, T.,
F. Kunst, and G. Rapoport.
1993.
Two-component regulatory systems, p. 729-745.
In
A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, D.C.
|
| 13.
|
Msadek, T.,
F. Kunst, and G. Rapoport.
1995.
A signal transduction network in Bacillus subtilis includes the DegS/DegU and ComP/ComA two-component systems, p. 447-471.
In
J. A. Hoch, and T. J. Silhavy (ed.), Two-component signal transduction. American Society for Microbiology, Washington, D.C.
|
| 14.
|
Mukai, K.,
M. Kawata, and T. Tanaka.
1990.
Isolation and phosphorylation of the Bacillus subtilis degS and degU gene products.
J. Biol. Chem.
265:824-834.
|
| 15.
|
Mukai, K.,
M. Kawata-Mukai, and T. Tanaka.
1992.
Stabilization of phosphorylated Bacillus subtilis DegU by DegR.
J. Bacteriol.
174:7954-7962[Abstract/Free Full Text].
|
| 16.
|
Nagami, Y., and T. Tanaka.
1986.
Molecular cloning and nucleotide sequence of a DNA fragment from Bacillus natto that enhances production of extracellular proteases and levansucrase in Bacillus subtilis.
J. Bacteriol.
166:20-28[Abstract/Free Full Text].
|
| 17.
|
Ogura, M.,
M. Kawata-Mukai,
M. Itaya,
K. Takio, and T. Tanaka.
1994.
Multiple copies of the proB gene enhance degS-dependent extracellular protease production in Bacillus subtilis.
J. Bacteriol.
176:5673-5680[Abstract/Free Full Text].
|
| 18.
|
Pang, A. S.-H.,
S. Nathoo, and S. Wong.
1991.
Cloning and characterization of a pair of novel genes that regulates production of extracellular enzymes in Bacillus subtilis.
J. Bacteriol.
173:46-54[Abstract/Free Full Text].
|
| 19.
|
Schaeffer, P. J.,
J. Millet, and J. Aubert.
1965.
Catabolite repression of bacterial sporulation.
Proc. Natl. Acad. Sci. USA
54:704-711[Free Full Text].
|
| 20.
|
Tanaka, T., and M. Kawata.
1988.
Cloning and characterization of Bacillus subtilis iep, which has positive and negative effects on production of extracellular proteases.
J. Bacteriol.
170:3593-3600[Abstract/Free Full Text].
|
| 21.
|
Tanaka, T.,
M. Kawata, and K. Mukai.
1991.
Altered phosphorylation of Bacillus subtilis DegU caused by single amino acid changes in DegS.
J. Bacteriol.
173:5507-5515[Abstract/Free Full Text].
|
| 22.
|
Ward, J. B., Jr., and S. A. Zahler.
1973.
Genetic studies of leucine biosynthesis in Bacillus subtilis.
J. Bacteriol.
116:719-726[Abstract/Free Full Text].
|
| 23.
|
Wendrich, T. M., and M. A. Marahiel.
1997.
Cloning and characterization of a relA/spoT homologue from Bacillus subtilis.
Mol. Microbiol.
26:65-79[CrossRef][Medline].
|
Journal of Bacteriology, August 2001, p. 4648-4651, Vol. 183, No. 15
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.15.4648-4651.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Arai, A., Kawachi, E., Hata, M., Ogura, M., Tanaka, T.
(2003). Inhibition of Bacillus subtilis aprE Expression by Lincomycin at the Posttranscriptional Level through Inhibition of ppGpp Synthesis. J Biochem
134: 691-697
[Abstract]
[Full Text]
-
Eymann, C., Homuth, G., Scharf, C., Hecker, M.
(2002). Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J. Bacteriol.
184: 2500-2520
[Abstract]
[Full Text]
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