TABLE 2.
List of B. subtilis genes exhibiting significantly increased mRNA levels during phosphate starvation conditions as determined by DNA macroarray analysis
| Gene | Potential Pho box sequences upstream of the start codon | Functiona | Fold induction ratiob
|
Transcriptional organizationa [reference(s)] | Secreted/nonsecreted proteinc | ||
|---|---|---|---|---|---|---|---|
| WT | phoR | sigB | |||||
| Previously identified PhoP regulon members | |||||||
| glpQ | Glycerophosphoryl diester phosphodiesterase | 10.0 | 3.9 | 38.2 | gplQ (7) | Secreted | |
| phoA | ATGATCAACAGCCGCATTTAACAAAG-T37 ATG | Alkaline phosphatase A | 36.9 | 1.2 | 132.1 | phoA (65) | Secreted |
| phoB | ATCTTTAAAATCGATTAATACTAG-N65 TTG | Alkaline phosphatase III | 183.3 | 1.7 | 166.2 | phoB-ydhF (7) | Secreted |
| phoD | TCAGTTCACACTTCTTCACAGTCG-N55 ATG | Phosphodiesterase/alkaline phosphatase | 59.0 | 2.8 | 51.9 | phoD-tatAD-tatCD (34) | Secreted |
| phoP | Two-component response regulator | 1.7 | 1.7 | 4.8 | phoP-phoR (56, 60) | Nonsecreted | |
| phoR | Two-component sensor histidine kinase | 1.9 | 0.5 | 3.6 | phoP-phoR (56, 60) | Nonsecreted | |
| pstA | Phosphate ABC transporter (permease) | 8.8 | 1.5 | 5.4 | pstS-pstC-pstA-pstBA-pstBB (3, 67) | Nonsecreted | |
| pstBA | Phosphate ABC transporter (ATP-binding protein) | 85.1 | 1.8 | 48.5 | pstS-pstC-pstA-pstBA-pstBB (3, 67) | Nonsecreted | |
| pstBB | Phosphate ABC transporter (ATP-binding protein) | 8.6 | 1.8 | 6.9 | pstS-pstC-pstA-pstBA-pstBB (3, 67) | Nonsecreted | |
| pstC | Phosphate ABC transporter (permease) | 31.0 | N/A | 18.8 | pstS-pstC-pstA-pstBA-pstBB (3, 67) | Nonsecreted | |
| pstS | CCTTTTTACATAGAACCTTTACTCTAT-N45 ATG | Phosphate ABC transporter (binding protein) | 32.1 | 1.5 | 18.1 | pstS-pstC-pstA-pstBA-pstBB (3, 67) | Secreted |
| resA | AAATTTCACATAACCTTCAAAAAGT-N64 GTG | Essential protein similar to cytochrome c biogenesis protein | 2.2 | 0.9 | 1.0 | resA-resB-resC-resD-resE (10) | Nonsecreted |
| resB | Required for cytochrome c synthesis | 0.8 | 0.6 | 0.7 | resA-resB-resC-resD-resE (10) | Nonsecreted | |
| resC | Required for cytochrome c synthesis | 1.1 | 0.8 | N/A | resA-resB-resC-resD-resE (10) | Nonsecreted | |
| resD | ACAGTTCTCAAACTTTCTCACGAT-N41 ATG | Two-component response regulator | 1.1 | 0.9 | 0.9 | resA-resB-resC-resD-resEresD-resE (10) | Nonsecreted |
| resE | Two-component sensor histidine kinase | 1.3 | 0.9 | 0.6 | resA-resB-resC-resD-resE resD-resE (10) | Nonsecreted | |
| tagA | Teichoic acid biosynthesis | 0.5 | 0.64 | N/A | tagA-tagB (44, 66) | Nonsecreted | |
| tagB | Involved in polyglycerol phosphate teichoic acid biosynthesis | 1.6 | 0.71 | N/A | tagA-tagB (44, 66) | Nonsecreted | |
| tagD | Glycerol-3-phosphate cytidylyltransferase | 0.4 | 0.47 | 1.7 | tagD-tagE-tagF (44, 66) | Nonsecreted | |
| tagE | UDP-glucose:polyglycerol phosphate glucosyltransferase | 0.4 | N/A | N/A | tagD-tagE-tagF (44, 66) | Nonsecreted | |
| tagF | N/A | N/A | N/A | tagD-tagE-tagF (44, 66) | Nonsecreted | ||
| tuaA | AGTATTAACAACATTTATCAGAAA-N11 GTG | Biosynthesis of teichuronic acid | 19.8 | 0.6 | 5.5 | tuaA-tuaB-tuaC-tuaD-tuaE-tuaF-tuaG-tuaH (37) | Nonsecreted |
| tuaB | Biosynthesis of teichuronic acid | 3.1 | 0.6 | 5.1 | tuaA-tuaB-tuaC-tuaD-tuaE-tuaF-tuaG-tuaH (37) | Nonsecreted | |
| tuaC | Biosynthesis of teichuronic acid | 23.1 | 1.8 | 7.6 | tuaA-tuaB-tuaC-tuaD-tuaE-tuaF-tuaG-tuaH (37) | Nonsecreted | |
| tuaD | Biosynthesis of teichuronic acid | 14.4 | 1.3 | 10.0 | tuaA-tuaB-tuaC-tuaD-tuaE-tuaF-tuaG-tuaH (37) | Nonsecreted | |
| tuaE | Biosynthesis of teichuronic acid | 10.4 | 0.8 | N/A | tuaA-tuaB-tuaC-tuaD-tuaE-tuaF-tuaG-tuaH (37) | Nonsecreted | |
| tuaF | Biosynthesis of teichuronic acid | 24.9 | 1.2 | 16.4 | tuaA-tuaB-tuaC-tuaD-tuaE-tuaF-tuaG-tuaH (37) | Nonsecreted | |
| tuaG | Biosynthesis of teichuronic acid | 15.3 | 2.6 | 18.1 | tuaA-tuaB-tuaC-tuaD-tuaE-tuaF-tuaG-tuaH (37) | Nonsecreted | |
| tuaH | Biosynthesis of teichuronic acid | 3.8 | 0.9 | 13.7 | tuaA-tuaB-tuaC-tuaD-tuaE-tuaF-tuaG-tuaH (37) | Nonsecreted | |
| tatAd | Similar to hypothetical proteins | 2.7 | 1.5 | 1.5 | phoD-tatAD-tatCD (34) | Nonsecreted | |
| ydhF | Similar to unknown proteins from B. subtilis | 76.9 | 0.72 | 43.9 | phoB-ydhF (7) | Secreted | |
| ykoL | ATTCTTTACATTAGATTCATACCAC-N56 ATG | Unknown | 3.6 | N/A | 3.2 | ykzB-ykoL ykoL (60) | Nonsecreted |
| yttP | Similar to unknown proteins | 1.2 | 0.8 | 1.3 | yttP | Nonsecreted | |
| Remaining wild-type genes | |||||||
| bpr | GTAATTCAGATTGTCTACAGTTA-N88 ATG | Bacillopeptidase F | 9.7 | 2.4 | 14.2 | bpr | Secreted |
| lytB | Modifier protein of major autolysin LytC | 52.8 | N/A | N/A | lytA-lytB-lytC (38) | Secreted | |
| rapA | Response regulator aspartate phosphatase | 8.7 | 6.0 | 7.6 | rapA-phrA (57) | Nonsecreted | |
| glcU | Glucose uptake | 5.3 | 1.3 | N/A | glcU-gdh (52) | Nonsecreted | |
| ydbD | Similar to manganese-containing catalase | 9.2 | 3.8 | 1.1 | ydbE-ydbD (8) | Nonsecreted | |
| cotP | Spore coat protein | 5.4 | 0.6 | N/A | cotP (68) | Nonsecreted | |
| yfkN | AATAGTTACAAAATATTCTTACAATAG-N3 GTG | Similar to 2′,3′-cyclic-nucleotide 2′-phosphodiesterase | 6.3 | 1.1 | 17.3 | yfkN | Secreted |
| yukJ | Unknown | 5.5 | 2.7 | 4.7 | yuxI-yukJ | Nonsecreted | |
| yxnB | Unknown | 9.8 | 3.5 | 18.5 | yxbB-yxbA-yxnB-asnH-yxaM (83) | Nonsecreted | |
| Genome-wide analysis of a phoR-null mutant | |||||||
| csbD | σB-transcribed gene | 1.7 | 29.7 | N/A | csbD (2) | Nonsecretoryprotein | |
| csbX | σB-transcribed gene | 1.1 | 6.0 | N/A | csbX-bofC(24) | Nonsecreted | |
| dps | Stress- and starvation-induced gene controlled by σB | 1.6 | 6.0 | N/A | dps (6) | Nonsecreted | |
| gsiB | General stress protein | 6.0 | 63.5 | 1.4 | gsiB (35) | Nonsecreted | |
| gspA | General stress protein | 2.6 | 19.8 | N/A | gspA (5) | Nonsecreted | |
| rsbW | Negative regulation of σB-dependent gene expression | 2.3 | 10.7 | 0.7 | rsbR-rsbS-rsbT-rsbU-rsbV-rsbW-sigB-rsbX rsbV-rsbW-sigB-rsbX (82) | Nonsecreted | |
| rsbX | Indirect negative regulation of σB-dependent gene expression | 1.8 | 5.8 | N/A | rsbR-rsbS-rsbT-rsbU-rsbV-rsbW-sigB-rsbXrsbV-rsbW-sigB-rsbX (82) | Nonsecreted | |
| skfA | GGGTTAAAATATTCTATTTATACTAA-N124 ATG | Unknown | 9.9 | 5.1 | 32.8 | skfA-skfB-skfC-skfD-skfE-skfF-skfG-skfH (25) | Nonsecreted |
| ybyB | Unknown | 8.5 | 29.0 | N/A | ybyB | Nonsecreted | |
| ycsD | Similar to hydroxymyristoyl-(acyl carrier protein) dehydratase | 6.0 | 8.6 | N/A | ycsD-ycsE | Nonsecreted | |
| ydaD | Similar to alcohol dehydrogenase | 2.0 | 10.2 | N/A | ydaD-ydaE (59) | Nonsecreted | |
| ydaE | Unknown | 3.3 | 97.6 | N/A | ydaD-ydaE (59) | Nonsecreted | |
| ydaP | Unknown | 2.8 | 11.2 | N/A | mutT-ydaP | Nonsecreted | |
| yfkJ | Similar to protein-tyrosine phosphatase | 1.9 | 6.9 | 1.5 | yfkJ-yfkI-yfkH | Nonsecreted | |
| yfkM | Similar to hypothetical proteins | 1.2 | 29.6 | N/A | yfkK-yfkL-yfkM (59) | Nonsecreted | |
| yflT | Unknown | 8.1 | 22.7 | 0.5 | yfmA-yflT | Nonsecreted | |
| ygxB | Similar to hypothetical proteins from B. subtilis | 2.2 | 16.7 | N/A | ygxB | Nonsecreted | |
| yheK | Similar to hypothetical proteins | 4.1 | 27.3 | N/A | yheK (61) | Nonsecreted | |
| yjbC | Induced by phosphate starvation in a σB-dependent and PhoPR-independent manner | 1.3 | 4.8 | 2.1 | yjbC-spx (yjbD) (7) | Nonsecreted | |
| ykzA | TTATTTTCCATTTTGTTCACCAACT-N124 ATG | Similar to general stress protein | 10.7 | 13.7 | N/A | ykzA (81) | Nonsecreted |
| yocB | Unknown | 2.3 | 7.4 | N/A | yocB | Nonsecreted | |
| yqgZ | Similar to hypothetical proteins | 5.1 | 9.1 | N/A | yqgZ | Nonsecreted | |
| yrzI | Unknown | 1.6 | 4.6 | N/A | yrzI | Nonsecreted | |
| ysnF | TATATTCACACATTTTTCACCTT-N68 ATG | Unknown | 1.6 | 27.0 | N/A | ysnF | Nonsecreted |
| ytxG | TATGTATACAGCCCAGTACACATGTT-N55 ATG | Similar to general stress protein | 1.1 | 21.7 | 1.7 | ytxG-ytxH-ytxJ | Nonsecreted |
| ytzE | Similar to transcriptional regulator | 4.7 | 12.9 | 7.7 | ytzE | Nonsecreted | |
| yvgO | Unknown | 1.5 | 5.0 | 0.6 | yvgO | Secreted | |
| yvyD | AAAGTTCACTGAATTTTCACAAA-N79 ATG | Similar to ribosomal protein S30AE family | 1.4 | 22.2 | 1.1 | yvyD (17) | Nonsecreted |
| ywzA | Similar to hypothetical proteins from B. subtilis | 4.9 | 36.6 | N/A | ywzA | Nonsecreted | |
| Genome-wide analysis of a sigB-null mutant | |||||||
| asnH | Asparagine synthetase | N/A | N/A | 259.4 | yxbB-yxbA-yxnB-asnH-yxaM (83) | Nonsecreted | |
| bpr | GTAATTCAGATTGTCTACAGTTA-N88 ATG | Bacillopeptidase F | 9.7 | 2.4 | 14.4 | Bpr | Secreted |
| metC | Methionine biosynthesis | 1.8 | 0.6 | 13.1 | metI-metC (9) | Nonsecreted | |
| pel | Pectate lyase | 4.0 | 2.2 | 4.0 | pel (53) | Secreted | |
| pksE | Involved in polyketide synthesis | 2.3 | 0.6 | 3.4 | pksB-pksC-pksD-pksE-acpK-pksF | Nonsecreted | |
| ppsA | Plipastatin synthetase | N/A | 1.6 | 4.7 | ppsA-ppsB-ppsC-ppsD-ppsE (77) | Nonsecreted | |
| rapA | Response regulator aspartate phosphatase | 8.7 | 6.2 | 7.6 | rapA-phrA (57) | Nonsecreted | |
| skfA | GGGTTAAAATATTCTATTTATACTAA-N124ATG | Unknown | 9.9 | 5.1 | 32.8 | skfA-skfB-skfC-skfD-skfE-skfF-skfG-skfH | Nonsecreted |
| spoIIAA | Stage II sporulation | N/A | N/A | 5.7 | spoIIAA-spoIIAB-sigF (70) | Nonsecreted | |
| spoIIB | Stage II sporulation | 4.3 | N/A | 9.9 | spoIIB | Nonsecreted | |
| srfAA | TTAGTTCATAAGAATTAAAAGCTG-N70 ATG | Surfactin production and competence | 2.2 | 1.0 | 3.3 | srfAA-srfAB-srfAC-srfAD | Nonsecreted |
| thrC | Threonine biosynthesis | 0.7 | 0.6 | 7.7 | hom-thrC-thrB (55) | Nonsecreted | |
| yfkN | ATAGTTACAAAATATTCTTACAATAG-N38GTG | Similar to 2′,3′-cyclic-nucleotide 2′-phosphodiesterase | 6.3 | 1.1 | 17.4 | yfkN | Secreted |
| yhcR | Similar to 5′-nucleotidase | 1.7 | 1.5 | 4.3 | yhcR-yhcS | Nonsecreted | |
| yhzC | CCGGTTTACGGCATTTTGCAGGAT-N105 ATG | Unknown | 2.0 | 1.2 | 6.5 | yhzC | Nonsecreted |
| yjdB | ATTATTAACATTTATTTACAAGGA-N63 ATG | Unknown | 2.6 | 0.8 | 5.1 | yjdB | Secreted |
| ykzF | Unknown | 1.5 | 2.9 | 3.9 | ykuJ-ykuK-ykzF-ykuL-ykuM | Nonsecreted | |
| yoeB | TATTGTAACATTTGTAACATAAG-N29 ATG | Unknown | 0.7 | N/A | 4.0 | yoeB | Nonsecreted |
| ytzE | Similar to transcriptional regulator (DeoR family) | 4.7 | 12.9 | 7.6 | ytzE | Nonsecreted | |
| yuiB | Similar to hypothetical proteins from B. subtilis | 2.7 | 2.3 | 11.6 | yuiA-yuiB | Nonsecreted | |
| yukJ | Unknown | 5.5 | 2.7 | 4.7 | yuxI-yukJ | Nonsecreted | |
| yuxI | Unknown | N/A | 1.8 | 8.4 | yuxI-yukJ | Nonsecreted | |
| ywkC | Unknown | 3.0 | 1.7 | 4.4 | ywkD-ywkC | Nonsecreted | |
| yxbB | Similar to hypothetical proteins | 4.9 | 6.2 | 26.9 | yxbB-yxbA-yxnB-asnH-yxaM (83) | Nonsecreted | |
| yxnB | Unknown | 9.8 | 3.5 | 18.2 | yxbB-yxbA-yxnB-asnH-yxaM (83) | Nonsecreted | |
| yycO | Unknown | 3.6 | N/A | 15.0 | yycO-yycP (20) | Secreted | |
a
Function and putative transcriptional organization are according to the associated reference. When no reference has been detected in the literature, the organization is according to the SubtiList database (http://genolist.pasteur.fr/SubtiList) (48). Gene names in parentheses are alternative names.
b
Calculated fold induction ratios (between pre- and postphosphate starvation) for genes averaged from two biologically independent experiments. Genes that fulfill the criteria for the outlier analysis are given in bold type and underlined. Genes that did not fulfill the outlier analysis criteria are shown as N/A. WT, wild type.
c
Whether the protein is predicted to be secreted or nonsecreted according to Tjalsma and coworkers (76).