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Table 3S: Transcriptome data summary for genes of the Arg, Cys and His biosynthesis pathways.
gene
description
Ag(I)
Arginine Biosynthesis
argC N-acetylglutamate gamma-semialdehyde
dehydrogenase
argJ
ornithine acetyltransferase
argB N-acetylglutamate 5-phosphotransferase
argD N-acetylornithine aminotransferase
carA
carbamoyl-phosphate transferase-arginine
carB
carbamoyl-phosphate transferase-arginine
argG argininosuccinate synthase
argH argininosuccinate lyase
yqiX
high affinity Arg transport
yqiY
high affinity Arg transport
yqiZ
high affinity Arg transport
As(V)
Fold induction1
Cd(II) Ni(II) Zn(II)
reference
Cu(II)
35.3
1.0
1.0
1.0
1.0
1.0 (Belitsky, 2002)
133.1
39.0
20.9
11.0
15.8
26.8
14.9
26.2
12.2
11.0
0.9
1.0
1.0
1.0
1.0
0.5
0.8
0.6
0.8
0.6
0.4
0.5
0.6
1.0
1.0
1.0
0.8
0.9
0.8
0.8
1.0
1.0
1.0
1.0
1.0
1.3
1.0
1.3
1.1
1.1
1.1
1.1
1.0
1.0
0.9
1.1
0.9
1.0
1.0
1.2
1.0
1.1
1.0
0.9
1.0
0.9
1.0
1.0
1.8
1.1
Cysteine Biosynthesis
cysH phosphoadenosine phosphosulfate
15.2
12.6
0.4
1.2
1.9
cysP
sulfate permease
27.0
16.8
0.4
1.2
2.9
sat
cysC
ylnD
ylnE
yrhA
yrhB
probable sulfate adenylyltransferase
probable adenylylsulfate kinase
uroporphyrin-III C-methyltransferase
unknown; cysH operon
similar to cysteine synthase
similar to cystathionine gamma-synthase
24.0
29.42
19.1
4.6
25.3
21.8
16.7
2.0
10.3
2.9
4.9
5.1
0.4
0.4
0.4
0.6
1.8
1.1
1.3
1.2
1.3
1.1
1.1
1.2
2.3
2.8
2.6
1.6
5.7
3.2
1.2 (Mansilla and de Mendoza,
1997)
1.5 (Mansilla and de Mendoza,
2000)
1.4 (Grundy and Henkin, 2002)
1.2 (Grundy and Henkin, 2002)
1.3 (Grundy and Henkin, 2002)
1.0 (Grundy and Henkin, 2002)
3.0 (Grundy and Henkin, 2002)
3.0 (Grundy and Henkin, 2002)
(Belitsky, 2002)
(Belitsky, 2002)
(Belitsky, 2002)
(Belitsky, 2002)
(Belitsky, 2002)
(Belitsky, 2002)
(Belitsky, 2002)
(Sekowska et al., 2001)
(Sekowska et al., 2001)
(Sekowska et al., 2001)
cysK
yxeK
yxeL
yxeM
yxeN
yxeO
yxeP
yhcL
yrrT
ytlI
cysteine synthetase A
similar to monooxygenase
similar to acetyltransferase
amino acid ABC transporter
amino acid ABC transporter
amino acid ABC transporter
similar to aminoacylase
similar to sodium-glutamate symporter
similar to SAM dep. methyltransferase
LysR family regulatory protein
Histidine Biosynthesis
hisZ
histidyl-tRNA synthetase
hisG
ATP phosphoribosyltransferase
hisD
histidinol dehydrogenase
hisB
imidazoleglycerol-phosphate dehydratase
hisH
amidotransferase
hisA
isomerase
hisF
HisF cyclase-like protein
hisI
pyrophosphohydrolase
yuiF
histidine transporter
7.7
18.5
34.1
18.7
6.9
14.9
15.4
20.9
5.4
29.2
10.2
3.9
5.9
4.7
1.6
2.7
1.3
3.4
1.4
2.4
0.6
1.3
1.1
0.8
0.7
1.2
0.9
0.9
1.2
3.2
1.2
1.0
1.5
1.6
1.1
1.1
1.0
1.1
1.2
1.0
1.6
4.8
8.8
2.2
2.4
2.2
4.0
6.2
2.04
4.9
2.8
3.1
3.0
2.3
1.7
1.8
1.4
3.0
3.2
3.0
(Grundy and Henkin, 2002)
(Auger et al., 2002)
(Auger et al., 2002)
(Auger et al., 2002)
(Auger et al., 2002)
(Auger et al., 2002)
(Auger et al., 2002)
(Burguiere et al., 2004)
(Grundy and Henkin, 2003)
(Coppee et al., 2001)
58.4
15.0
57.4
47.0
39.4
31.1
26.4
8.6
21.4
1.0
1.6
1.0
1.0
1.0
1.0
1.0
1.0
0.5
0.7
0.7
0.9
0.9
0.4
0.4
0.4
0.6
0.9
2.7
1.8
4.1
5.3
4.2
5.7
6.7
2.8
2.4
1.5
1.3
2.1
0.9
1.0
1.3
1.0
1.0
1.8
2.8
1.7
3.6
4.5
2.1
3.9
3.1
2.0
4.2
(Sonenshein, 1993)
(Sonenshein, 1993)
(Sonenshein, 1993)
(Sonenshein, 1993)
(Sonenshein, 1993)
(Sonenshein, 1993)
(Sonenshein, 1993)
(Sonenshein, 1993)
(Vitreschak et al., 2004)
Fold induction by 3 min. metal stress at OD600=0.3 in LB medium at the following concentrations: 10 M Ag(II); 10 M As(V); 10
M Cd(II); 10 M Cu(II); 500 M Ni(II) or 300 M Zn(II).
1
Genes included for each pathway were: Arg (argCJBDcarAB, argGHytzD, yqiXYZ), Cys
(cysHcysP(ylnA)sat(ylnB)cysC(ylnC)ylnDE, yrhAB, cysK, yxeKLMNOP, yhcL, yrrT, ytlI) and His (hisZGDBHAFI, yuiF). The argC
operon encodes the enzyme for synthesis of citrulline which is converted to Arg by the products of the argGH genes (Belitsky, 2002).
The yqiXYZ operon encodes a high affinity Arg transport system (Sekowska et al., 2001).The cysH operon together with cysK encodes
enzymes for the synthesis of Cys from sulfate and O-acetylserine and the yrhAB genes encode the cystathionine -synthase and lyase for conversion of homocysteine to Cys (Grundy and Henkin, 2002). The yrrT gene is located upstream of the yrhAB genes,
appears to be regulated by a Met-specific antitermination mechanism (T-box; (Grundy and Henkin, 2003) and is postulated to function
in a reverse pathway of synthesis of Cys from Met (Rodionov et al., 2004). The yxeK operon, yhcL, and ytlI are known to be strongly
up-regulated during growth on methionine as sole sulfur source (relative to sulfate-grown cells; (Auger et al., 2002) . YhcL is a
symporter that functions in the uptake of cystine and has been renamed TcyP (Burguiere et al., 2004). The YtlI protein functions as a
positive activator of the divergent ytmI operon (although this operon was not induced under the tested conditions) which is apparently
involved in some aspect of sulfur assimilation (Coppee et al., 2001). The hisZ operon encodes the major enzymes for His biosynthesis
and YuiF has recently been proposed to be a histidine transporter (Vitreschak et al., 2004). Note that not all genes in every predicted
operon made the 5-fold cut-off for inclusion in this analysis. Further, many genes regulated by the SAM-dependent S-box termination
mechanism (Grundy and Henkin, 2003) were not detected as strongly regulated in this analysis.
References
Auger, S., Danchin, A., and Martin-Verstraete, I. (2002) Global expression profile of Bacillus subtilis grown in the presence of
sulfate or methionine. J Bacteriol 184: 5179-5186.
Belitsky, B.R. (2002) Biosynthesis of Amino Acids of the Glutamate and Aspartate Families, Alanine, and Polyamines. In
Bacillus subtilis and its closest relatives. Sonenshein, A.L., Hoch, J.A. and Losick, R. (eds). Washington, D. C.: ASM
Press, pp. 203-231.
Burguiere, P., Auger, S., Hullo, M.F., Danchin, A., and Martin-Verstraete, I. (2004) Three different systems participate in Lcystine uptake in Bacillus subtilis. J Bacteriol 186: 4875-4884.
Coppee, J.Y., Auger, S., Turlin, E., Sekowska, A., Le Caer, J.P., Labas, V., Vagner, V., Danchin, A., and Martin-Verstraete, I.
(2001) Sulfur-limitation-regulated proteins in Bacillus subtilis: a two-dimensional gel electrophoresis study.
Microbiology 147: 1631-1640.
Grundy, F.J., and Henkin, T.M. (2002) Synthesis of Serine, Glycine, Cysteine, and Methionine. In Bacillus subtilis and its
closest relatives. Sonenshein, A.L., Hoch, J.A. and Losick, R. (eds). Washington, D. C.: ASM Press, pp. 245-254.
Grundy, F.J., and Henkin, T.M. (2003) The T box and S box transcription termination control systems. Front Biosci 8: d20-31.
Mansilla, M.C., and de Mendoza, D. (1997) L-cysteine biosynthesis in Bacillus subtilis: identification, sequencing, and
functional characterization of the gene coding for phosphoadenylylsulfate sulfotransferase. J Bacteriol 179: 976-981.
Mansilla, M.C., and de Mendoza, D. (2000) The Bacillus subtilis cysP gene encodes a novel sulphate permease related to the
inorganic phosphate transporter (Pit) family. Microbiology 146 ( Pt 4): 815-821.
Rodionov, D.A., Vitreschak, A.G., Mironov, A.A., and Gelfand, M.S. (2004) Comparative genomics of the methionine
metabolism in Gram-positive bacteria: a variety of regulatory systems. Nucleic Acids Res 32: 3340-3353.
Sekowska, A., Robin, S., Daudin, J.J., Henaut, A., and Danchin, A. (2001) Extracting biological information from DNA arrays:
an unexpected link between arginine and methionine metabolism in Bacillus subtilis. Genome Biol 2: RESEARCH0019.
Sonenshein, A.L. (1993) Introduction to Metabolic Pathways. In Bacillus subtilis and other Gram-Positive Bacteria. Sonenshein,
A.L., Hoch, J.A. and Losick, R. (eds). Washington, D.C.: ASM Press.
Vitreschak, A.G., Lyubetskaya, E.V., Shirshin, M.A., Gelfand, M.S., and Lyubetsky, V.A. (2004) Attenuation regulation of
amino acid biosynthetic operons in proteobacteria: comparative genomics analysis. FEMS Microbiol Lett 234: 357-370.