The two-component system PhoPR of Clostridium acetobutylicum is involved in phosphate-dependent gene regulation

Journal of Bacteriology

Volumn 190, Issue 20, 2008, Pages 6559-6567

  Fiedler, Tomas ^a   Mix, Maren ^a   Meyer, Uta ^a,b   Mikkat, Stefan ^a   Glocker, Michael O ^a   Bahl, Hubert ^a   Fischer, Ralf Jorg ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b SANOFI AVENTIS DEUTSCHLAND GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATE;

ARTICLE; AUTOPHOSPHORYLATION; BACTERIAL GENE; BACTERIUM CULTURE; CLOSTRIDIUM ACETOBUTYLICUM; CONTROLLED STUDY; ESCHERICHIA COLI; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENETIC TRANSCRIPTION; NONHUMAN; OPERON; PHOP GENE; PHOR GENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; TWO DIMENSIONAL GEL ELECTROPHORESIS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; CLOSTRIDIUM ACETOBUTYLICUM; DNA, BACTERIAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENE ORDER; MOLECULAR SEQUENCE DATA; PHOSPHATES; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION SITE;

CLOSTRIDIUM ACETOBUTYLICUM; CLOSTRIDIUM ACETOBUTYLICUM ATCC 824; ESCHERICHIA COLI;

EID: 53849098363     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00574-08     Document Type: Article

References (59)

1. S+V promoters during Pho response. J. Bacteriol. 187:5166-5178.
2. Aguena, M., E. Yagil, and B. Spira. 2002. Transcriptional analysis of the pst operon of Escherichia coli. Mol. Genet. Genomics 268:518-524.
3. Allenby, N. E. E., N. O'Connor, Z. Prágai, A. C. Ward, A. Wipat, and C. R. Harwood. 2005. Genome-wide transcriptional analysis of the phosphate starvation stimulon of Bacillus subtilis. J. Bacteriol. 187:8063-8080.
4. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res. 25:3389-3402.
5. Antelmann, H., C. Scharf, and M. Hecker. 2000. Phosphate starvation-inducible proteins of Bacillus subtilis: proteomics and transcriptional analysis. J. Bacteriol. 182:4478-4490.
6. Aravind, L., and C. P. Ponting. 1999. The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol. Lett. 176:111-116.
7. Bahl, H., W. Andersch, and G. Gottschalk. 1982. Continuous production of acetone and butanol by Clostridium acetobutylicum in a two-stage phosphate limited chemostat. Eur. J. Appl. Microbiol. Biotechnol. 15:201-205 (Erratum, 17:73, 1983.)
8. Bieleski, R. L. 1973. Phosphate pools, phosphate transport, and phosphate availability. Annu. Rev. Plant Physiol. 24:225-252.
9. Bookstein, C., C. W. Edwards, N. V. Kapp, and F. M. Hulett. 1990. The Bacillus subtilis 168 alkaline phosphatase III gene: impact of a phoAIII mutation on total alkaline phosphatase synthesis. J. Bacteriol. 172:3730-3737.
10. Bradford, M. M. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal. Biochem. 72:248-254.
11. Dürre, P., and H. Bahl. 1996. Microbial production of acetone/butanol/ isopropanol, p. 229-268. In P. Stadler (ed.), Biotechnology: a multi-volume comprehensive treatise, 2nd ed., vol. 1. VCH Verlagsgesellschaft, Weinheim, Germany.
12. Eder, S., W. Liu, and F. M. Hulett. 1996. A Bacillus subtilis secreted phosphodiesterase/alkaline phosphatase is the product of a Pho regulon gene, phoD. Microbiology 142:2041-2047.
13. Fischer, R.-J., and H. Bahl. 2005. Transport of phosphate, p. 287-294. In P. Dürre (ed.), Handbook on clostridia. CRC Press, Taylor and Francis Group, Boca Raton, FL.
14. Fischer, R.-J., S. Oehmcke, U. Meyer, K. Schwarz, M. Mix, T. Fiedler, and H. Bahl. 2006. Transcription of the pst operon of Clostridium acetobutylicum is dependent on phosphate concentration and pH. J. Bacteriol. 188:5469-5478.
15. Fulda, S., S. Mikkat, F. Huang, J. Huckauf, K. Marin, B. Norling, and M. Hagemann. 2006. Proteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC6803. Proteomics 6:2733-2745.
16. Ghorbel, S., J. Kormanec, A. Artus, and M.-J. Virolle. 2006. Transcriptional studies and regulatory interactions between the phoR-phoP operon and the phoU, mtpA, and ppk genes of Streptomyces lividans TK24. J. Bacteriol. 188:677-686.
17. Gorham, H. C., S. J. McGowan, P. R. H. Robson, and D. A. Hodgson. 1996. Light-induced carotenogenesis in Myxococcus xanthus: light-dependent membrane sequestration of ECF sigma factor CarQ by anti-sigma factor CarR. Mol. Microbiol. 19:171-186.
18. Helmann, J. D., and C. P. Moran, Jr. 2002. RNA polymerase and sigma factors, p. 289-312. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, DC.
19. Hulett, F. M., E. E. Kim, C. Bookstein, N. V. Kapp, C. W. Edwards, and H. W. Wyckoff. 1991. Bacillus subtilis alkaline phophatases III and IV: cloning, sequencing, and comparisons of deduced amino acid sequence with Escherichia coli alkaline phosphatase three-dimensional structure. J. Biol. Chem. 266:1077-1084.
20. Hulett, F. M. 2002. The Pho regulon, p. 193-201. In A. L. Sonenshein, J. A. Hoch, and R. Losick (ed.), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, DC.
21. Hulko, M., F. Berndt, M. Gruber, J. U. Linder, V. Truffault, A. Schultz, J. Martin, J. E. Schultz, A. N. Lupas, and M. Coles. 2006. The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929-940.
22. Inokuchi, Y. A. Hirashima, Y. Semine, L. Janosi, and A. Kaji. 2000. Role of ribosome recycling factor in translational coupling. EMBO J. 19:3788-3798.
23. Just, T., E. Gafumbegete, J. Gramberg, I. Prüfer, B. Ringel, S. Mikkat, H. W. Pau, and M. O. Glocker. 2006. Differential proteome analysis of tonsils from children with chronic tonsillitis in comparison with hyperplasia reveals disease-associated protein expression differences. Anal. Bioanal. Chem. 384:1134-1144.
24. Khorchid, A., and M. Ikura. 2006. Bacterial histidine kinase as signal sensor and transducer. Int. J. Biochem. Cell. Biol. 38:307-312.
25. Kimura, S., K. Makino, H. Shinagawa, M. Amemura, and A. Nakata. 1989. Regulation of the phosphate regulon of Escherichia coli: characterization of the promoter of the pstS gene. Mol. Gen. Genet. 215:374-380.
26. Kočan, M., S. Schaffer, T. Ishige, U. Sorger-Herrmann, V. F. Wendisch, and M. Bott. 2006. Two-component systems of Corynebacterium glutamicum: deletion analysis and involvement of the PhoS-PhoR system in the phosphate starvation response. J. Bacteriol. 188:724-732.
27. Liu, W., and F. M. Hulett. 1997. Bacillus subtilis PhoP binds to the phoB tandem promoter exclusively within the phosphate starvation-inducible promoter. J. Bacteriol. 179:6302-6310.
28. Liu, W., S. Eder, and F. M. Hulett. 1998. Analysis of Bacillus subtilis tagAB and tagDEF expression during phosphate starvation identifies a repressor role of PhoP-P. J. Bacteriol. 180:753-758.
29. Liu, W., and F. M. Hulett. 1998. Comparison of PhoP binding to the tuaA promoter with PhoP binding to other Pho-regulon promoters establishes a Bacillus subtilis Pho core binding site. Microbiology 144:1443-1450.
30. Makino, K., H. Shinagawa, M. Amemura, and A. Nakata. 1986. Nucleotide sequence of the phoB gene, the positive regulatory gene for the phosphate regulon of Escherichia coli K-12. J. Mol. Biol. 190:37-44.
31. Makino, K., H. Shinagawa, M. Amemura, and A. Nakata. 1986. Nucleotide sequence of the phoR gene, a regulatory gene for the phosphate regulon of Escherichia coli. J. Mol. Biol. 192:549-556.
32. May, A., F. Hillmann, O. Riebe, R.-J. Fischer, and H. Bahl. 2004. A rubrerythrin-like oxidative stress protein of Clostridium acetobutylicum is encoded by a duplicated gene and identical to the heat shock protein Hsp21. FEMS Microbiol. Lett. 238:249-254.
33. Meinecke, B., H. Bahl, and G. Gottschalk. 1984. Selection of an asporogenous strain of Clostridium acetobutylicum in continuous culture under phosphate limitation. Appl. Environm. Microbiol. 48:1064-1065.
34. Merighi, M., A. Carroll-Portillo, A. N. Septer, A. Bhatiya, and J. S. Gunn. 2006. Role of Salmonella enterica serovar Typhimurium two-component system PreA/PreB in modulatine PmrA-regulated gene transcription. J. Bacteriol. 188:141-149.
35. Mitchell, W. J. 2001. Spores and sporulation, p. 72-83. In P. Dürre (ed.), Clostridia: biotechnology and medical applications. Wiley-VCH Verlag GmbH, Weinheim, Germany.
36. 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.), 2Bacillus subtilis and other gram-positive bacteria: biochemistry, physiology, and molecular genetics. American Society for Microbiology, Washington, DC.
37. Neuhoff, V., N. Arold, D. Taube, and W. Ehrhardt. 1988. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9:255-262.
38. Nölling, J., G. Breton, M. V. Omelchenko, K. S. Marakowa, Q. Zeng, R. Gibson, H. M. Lee, J. Dubios, D. Qiu, and J. Hitti. 2001. Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J. Bacteriol. 183:4823-4838.
39. Nordhoff, E., M. Schurenberg, G. Thiele, C. Lubbert, K. D. Kloeppel, D. Theiss, H. Lehrach, and J. Gobom. 2003. Sample preparation protocols for MALDI-MS of peptides and oligonucleotides using prestructured sample supports. Int. J. Mass Spectrom. 226:163-180.
40. Oelmüller, U., N. Krüger, A. Steinbüchel, and C. G. Freidrich. 2002. Isolation of prokaryotic RNA and detection of specific mRNA with biotinylated probes. J. Microbiol. Methods 11:73-81.
41. Oultram, J. D., M. Loughlin, T.-J. Swinfield, J. K. Brehm, D. E. Thompson, and N. P. Minton. 1988. Introduction of plasmids into whole cells of Clostridium acetobutylicum by electroporation. FEMS Microbiol. Lett. 56:83-88.
42. Paul, S., S. Birkey, W. Liu, and F. M. Hulett. 2004. Autoinduction of Bacillus subtilis phoPR operon transcription results from enhanced transcription from EA- and EE-responsive promoters by phosphorylated PhoP. J. Bacteriol. 186:4262-4275.
43. Prágai, Z., N. N. E. Allenby, N. O'Connor, S. Dubrac, G. Rapoport, T. Msadek, C., and R. Harwood. 2004. Transcriptional regulation of the phoPR operon in Bacillus subtilis. J. Bacteriol. 186:1182-1190.
44. Qi, Y., Y. Kobayashi, and F. M. Hulett. 1997. The pst operon of Bacillus subtilis has a phosphate-regulated promoter and is involved in phosphate transport but not in regulation of the Pho regulon. J. Bacteriol. 179:2534-2539.
45. Qi, Y., and F. M. Hulett. 1998. Role of PhoP-P in transcriptional regulation of genes involved in cell wall anionic polymer biosynthesis in Bacillus subtilis. J. Bacteriol. 180:4007-4010.
46. Rao, N. N., and A. Torriani. 1990. Molecular aspects of phosphate transport in Escherichia coli. Mol. Microbiol. 4:1083-1090.
47. Rogers, P. G., and G. Gottschalk. 1993. Biochemistry and regulation of acid and solvent formation in clostridia, p. 25-50. In D. R. Woods (ed.), The clostridia and biotechnology. Butterworth-Heinemann, London, United Kingdom.
48. Schwarz, K., T. Fiedler, R.-J. Fischer, and H. Bahl. 2007. A standard operating procedure (SOP) for preparation of intra- and extracellular proteins of Clostridium acetobutylicum for proteome analysis. J. Microbiol. Methods 68:396-402.
49. Seki, T., H. Yoshikawa, H. Takahashi, and H. Saito. 1987. Cloning and nucleotide sequence of phoP, the regulatory gene for alkaline phosphatase and phosphodiesterase in Bacillus subtilis. J. Bacteriol. 169:2913-2916.
50. Seki, T., H. Yoshikawa, H. Takahashi, and H. Saito. 1988. Nucleotide sequence of the Bacillus subtilis phoR gene. J. Bacteriol. 170:5935-5938.
51. Shi, L., and F. M. Hulett. 1999. The cytoplasmic kinase domain of PhoR is sufficient for the low phosphate-inducible expression of Pho regulon genes in Bacillus subtilis. Mol. Microbiol. 31:211-222.
52. Sonenshein, A. L., J. D. Haraldsen, and B. Dupuy. 2005. RNA polymerase and alternative factors, p. 607-629. In P. Dürre (ed.), Handbook on clostridia. CRC Press, Taylor and Francis Group, Boca Raton, FL.
53. Sun, G., S. M. Birkey, and F. M. Hulett. 1996. Three two-component signal-transduction systems interact for Pho regulation in Bacillus subtilis. Mol. Microbiol. 19:941-948.
54. Supply, P., J. Magdalena, S. Himpens, and C. Locht. 1997. Identification of novel intergenic repetitive units in a mycobacterial two-component system operon. Mol. Microbiol. 26:991-1003.
55. Wanner, B. L. 1996. Phosphorus Assimilation and Control of the Phosphate Regulon, p. 1357-1381. 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. ASM Press, Washington, DC.
56. Watson, G. M. F., D. J. Scanlan, and N. H. Mann. 1996. Characterization of the genes encoding a phosphate-regulated two-component sensory system in the marine cyanobacterium Synechococcus sp. WH7803. FEMS Microbiol. Lett. 142:105-109.
57. Yarwood, J. M., J. K. McCormick, and P. M. Schlievert. 2001. Identification of a novel two-component regulatory system that acts in global regulation of virulence factors of Staphylococcus aureus. J. Bacteriol. 183:1113-1123.
58. Zhulin, I. B., B. L. Taylor, and R. Dixon. 1997. PAS-domain S-boxes in archaea, bacteria and sensors for oxygen and redox. Trends Biochem. Sci. 22:331-333.
59. Zilversmit, D. B., and A. K. Davis. 1950. Microdetermination of plasma phospholipids by trichloroacetic acid precipitation. J. Lab. Clin. Med. 35:155-160.