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Volume 151, Issue 11

YvcK of is required for a normal cell shape and for growth on Krebs cycle intermediates and substrates of the pentose phosphate pathway Free

Abstract

The HPr-like protein Crh has so far been detected only in the bacillus group of bacteria. In , its gene is part of an operon composed of six ORFs, three of which exhibit strong similarity to genes of unknown function present in many bacteria. The promoter of the operon was determined and found to be constitutively active. A deletion analysis revealed that gene , encoded by this operon, is essential for growth on Krebs cycle intermediates and on carbon sources metabolized via the pentose phosphate pathway. In addition, cells lacking YvcK acquired media-dependent filamentous or L-shape-like aberrant morphologies. The presence of high magnesium concentrations restored normal growth and cell morphology. Furthermore, suppressor mutants cured from these growth defects appeared spontaneously with a high frequency. Such suppressing mutations were identified in a transposon mutagenesis screen and found to reside in seven different loci. Two of them mapped in genes of central carbon metabolism, including , which encodes glucose-6-phosphate dehydrogenase and , the product of which regulates the synthesis of glyceraldehyde-3-phosphate dehydrogenase. All these results suggest that YvcK has an important role in carbon metabolism, probably in gluconeogenesis required for the synthesis of cell wall precursor molecules. Interestingly, the homologous protein, YbhK, can substitute for YvcK in , suggesting that the two proteins have been functionally conserved in these different bacteria.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): EMP, Embden–Meyerhoff–Parnas , mTn10, mini-Tn10 , PPP, pentose phosphate pathway and ST-PCR, semi-random, two-step PCR
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2005-11-01
2024-04-25
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References

  1. Antelmann H., Tjalsma H., Voigt B., Ohlmeier S., Bron S., van Dijl J. M., Hecker M. 2001; A proteomic view on genome-based signal peptide predictions. Genome Res 11:1484–1502 [CrossRef]
     [Google Scholar]
  2. Asai K., Baik S. H., Kasahara Y., Moriya S., Ogasawara N. 2000; Regulation of the transport system for C4-dicarboxylic acids in Bacillus subtilis . Microbiology 146:263–271
     [Google Scholar]
  3. Ayora S., Rojo F., Ogasawara N., Nakai S., Alonso J. C. 1996; The Mfd protein of Bacillus subtilis 168 is involved in both transcription-coupled DNA repair and DNA recombination. J Mol Biol 256:301–318 [CrossRef]
     [Google Scholar]
  4. Bachmann B. J. 1972; Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriol Rev 36:525–557
     [Google Scholar]
  5. Bagyan I., Hobot J., Cutting S. 1996; A compartmentalized regulator of developmental gene expression in Bacillus subtilis . J Bacteriol 178:4500–4507
     [Google Scholar]
  6. Boël G., Mijakovic I., Maze A. 7 other authors 2003; Transcription regulators potentially controlled by HPr kinase/phosphorylase in Gram-negative bacteria. J Mol Microbiol Biotechnol 5:206–215 [CrossRef]
     [Google Scholar]
  7. Bolhuis A., Broekhuizen C. P., Sorokin A., van Roosmalen M. L., Venema G., Bron S., Quax W. J., van Dijl J. M. 1998; SecDF of Bacillus subtilis , a molecular Siamese twin required for the efficient secretion of proteins. J Biol Chem 273:21217–21224 [CrossRef]
     [Google Scholar]
  8. Butland G., Peregrin-Alvarez J. M., Li J. 11 other authors 2005; Interaction network containing conserved and essential protein complexes in Escherichia coli . Nature 433:531–537 [CrossRef]
     [Google Scholar]
  9. Chun K. T., Edenberg H. J., Kelley M. R., Goebl M. G. 1997; Rapid amplification of uncharacterized transposon-tagged DNA sequences from genomic DNA. Yeast 13:233–240 [CrossRef]
     [Google Scholar]
  10. Cutting S. M., Vander Horn P. B. 1990; Genetic analysis. In Molecular Biological Methods for Bacillus Edited by Harwood C. R., Cutting S. M. Chichester: Wiley;
     [Google Scholar]
  11. Deutscher J., Galinier A., Martin-Verstraete I. 2002; Carbohydrate uptake and metabolism. In Bacillus subtilis and its Closest Relatives . pp 129–150 Edited by Sonnenshein A. L., Hoch J. A., Losick R. Washington, DC: American Society for Microbiology;
  12. Duong F., Wickner W. 1997; The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J 16:4871–4879 [CrossRef]
     [Google Scholar]
  13. Fillinger S., Boschi-Muller S., Azza S., Dervyn E., Branlant G., Aymerich S. 2000; Two glyceraldehyde-3-phosphate dehydrogenases with opposite physiological roles in a nonphotosynthetic bacterium. J Biol Chem 275:14031–14037 [CrossRef]
     [Google Scholar]
  14. Formstone A., Errington J. 2005; A magnesium-dependent mreB null mutant: implications for the role of mreB in Bacillus subtilis . Mol Microbiol 55:1646–1657 [CrossRef]
     [Google Scholar]
  15. Galinier A., Haiech J., Kilhoffer M. C., Jaquinod M., Stülke J., Deutscher J., Martin-Verstraete I. 1997; The Bacillus subtilis crh gene encodes a HPr-like protein involved in carbon catabolite repression. Proc Natl Acad Sci U S A 94:8439–8444 [CrossRef]
     [Google Scholar]
  16. Gilpin R. W., Young F. E., Chatterjee A. N. 1973; Characterization of a stable L-form of Bacillus subtilis 168. J Bacteriol 113:486–499
     [Google Scholar]
  17. Görke B., Fraysse L., Galinier A. 2004; Drastic differences in Crh and HPr synthesis levels reflect their different impacts on catabolite repression in Bacillus subtilis . J Bacteriol 186:2992–2995 [CrossRef]
     [Google Scholar]
  18. Graupner M., Xu H., White R. H. 2002; Characterization of the 2-phospho-l-lactate transferase enzyme involved in coenzyme F(420) biosynthesis in Methanococcus jannaschii . Biochemistry 41:3754–3761 [CrossRef]
     [Google Scholar]
  19. Helmann J. D., Moran C. P. 2002; RNA polymerase and sigma factors. In Bacillus subtilis and its Closest Relatives . pp 289–312 Edited by Sonnenshein A. L., Hoch J. A., Losick R. Washington, DC: American Society for Microbiology;
  20. Hilden I., Krath B. N., Hove-Jensen B. 1995; Tricistronic operon expression of the genes gcaD ( tms ), which encodes N -acetylglucosamine 1-phosphate uridyltransferase, prs , which encodes phosphoribosyl diphosphate synthetase, and ctc in vegetative cells of Bacillus subtilis . J Bacteriol 177:7280–7284
     [Google Scholar]
  21. Hirose I., Sano K., Shioda I., Kumano M., Nakamura K., Yamane K. 2000; Proteome analysis of Bacillus subtilis extracellular proteins: a two-dimensional protein electrophoretic study. Microbiology 146:65–75
     [Google Scholar]
  22. Ito M., Guffanti A. A., Oudega B., Krulwich T. A. 1999; mrp , a multigene, multifunctional locus in Bacillus subtilis with roles in resistance to cholate and to Na+ and in pH homeostasis. J Bacteriol 181:2394–2402
     [Google Scholar]
  23. Ito M., Guffanti A. A., Krulwich T. A. 2001; Mrp-dependent Na(+)/H(+) antiporters of Bacillus exhibit characteristics that are unanticipated for completely secondary active transporters. FEBS Lett 496:117–120 [CrossRef]
     [Google Scholar]
  24. Jolliffe L. K., Doyle R. J., Streips U. N. 1981; The energized membrane and cellular autolysis in Bacillus subtilis . Cell 25:753–763 [CrossRef]
     [Google Scholar]
  25. Joseph P., Fantino J. R., Herbaud M. L., Denizot F. 2001; Rapid orientated cloning in a shuttle vector allowing modulated gene expression in Bacillus subtilis . FEMS Microbiol Lett 205:91–97 [CrossRef]
     [Google Scholar]
  26. Kemper M. A., Urrutia M. M., Beveridge T. J., Koch A. L., Doyle R. J. 1993; Proton motive force may regulate cell wall-associated enzymes of Bacillus subtilis . J Bacteriol 175:5690–5696
     [Google Scholar]
  27. Kobayashi K., Ehrlich S. D., Albertini A. 96 other authors 2003; Essential Bacillus subtilis genes. Proc Natl Acad Sci U S A 100:4678–4683 [CrossRef]
     [Google Scholar]
  28. Krulwich T. A., Ito M., Guffanti A. A. 2001; The Na(+)-dependence of alkaliphily in Bacillus . Biochim Biophys Acta 1505158–168 [CrossRef]
     [Google Scholar]
  29. Kunst F., Rapoport G. 1995; Salt stress is an environmental signal affecting degradative enzyme synthesis in Bacillus subtilis . J Bacteriol 177:2403–2407
     [Google Scholar]
  30. Lazarevic V., Soldo B., Medico N., Pooley H., Bron S., Karamata D. 2005; Bacillus subtilis alpha-phosphoglucomutase is required for normal cell morphology and biofilm formation. Appl Environ Microbiol 71:39–45 [CrossRef]
     [Google Scholar]
  31. Ludwig H., Homuth G., Schmalisch M., Dyka F. M., Hecker M., Stülke J. 2001; Transcription of glycolytic genes and operons in Bacillus subtilis : evidence for the presence of multiple levels of control of the gapA operon. Mol Microbiol 41:409–422 [CrossRef]
     [Google Scholar]
  32. Martin-Verstraete I., Débarbouillé M., Klier A., Rapoport G. 1990; Levanase operon of Bacillus subtilis includes a fructose-specific phosphotransferase system regulating the expression of the operon. J Mol Biol 214:657–671 [CrossRef]
     [Google Scholar]
  33. Meinken C., Blencke H. M., Ludwig H., Stülke J. 2003; Expression of the glycolytic gapA operon in Bacillus subtilis : differential syntheses of proteins encoded by the operon. Microbiology 149:751–761 [CrossRef]
     [Google Scholar]
  34. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  35. Popham D. L., Stragier P. 1991; Cloning, characterization, and expression of the spoVB gene of Bacillus subtilis . J Bacteriol 173:7942–7949
     [Google Scholar]
  36. Prasad C., Freese E. 1974; Cell lysis of Bacillus subtilis caused by intracellular accumulation of glucose-1-phosphate. J Bacteriol 118:1111–1122
     [Google Scholar]
  37. Rasko D. A., Ravel J., Økstad O. A. 12 other authors 2004; The genome sequence of Bacillus cereus ATCC 10987 reveals metabolic adaptations and a large plasmid related to Bacillus anthracis pXO1. Nucleic Acids Res 32:977–988 [CrossRef]
     [Google Scholar]
  38. Roberts J., Park J. S. 2004; Mfd, the bacterial transcription repair coupling factor: translocation, repair and termination. Curr Opin Microbiol 7:120–125 [CrossRef]
     [Google Scholar]
  39. Saier M. H., Goldman S. R., Maile R. R., Moreno M. S., Weyler W., Yang N., Paulsen I. T Jr. 2002; Transport capabilities encoded within the Bacillus subtilis genome. J Mol Microbiol Biotechnol 4:37–67
     [Google Scholar]
  40. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  41. Schaeffer P., Millet J., Aubert J. P. 1965; Catabolic repression of bacterial sporulation. Proc Natl Acad Sci U S A 54:704–711 [CrossRef]
     [Google Scholar]
  42. Song B. H., Neuhard J. 1989; Chromosomal location, cloning and nucleotide sequence of the Bacillus subtilis cdd gene encoding cytidine/deoxycytidine deaminase. Mol Gen Genet 216:462–468 [CrossRef]
     [Google Scholar]
  43. Stülke J., Martin-Verstraete I., Zagorec M., Rose M., Klier A., Rapoport G. 1997; Induction of the Bacillus subtilis ptsGHI operon by glucose is controlled by a novel antiterminator, GlcT. Mol Microbiol 25:65–78 [CrossRef]
     [Google Scholar]
  44. Tanaka K., Kobayashi K., Ogasawara N. 2003; The Bacillus subtilis YufLM two-component system regulates the expression of the malate transporters MaeN (YufR) and YflS, and is essential for utilization of malate in minimal medium. Microbiology 149:2317–2329 [CrossRef]
     [Google Scholar]
  45. Vagner V., Dervyn E., Ehrlich S. D. 1998; A vector for systematic gene inactivation in Bacillus subtilis . Microbiology 144:3097–3104 [CrossRef]
     [Google Scholar]
  46. Veith B., Herzberg C., Steckel S. 9 other authors 2004; The complete genome sequence of Bacillus licheniformis DSM13, an organism with great industrial potential. J Mol Microbiol Biotechnol 7:204–211 [CrossRef]
     [Google Scholar]
  47. Wacker I., Ludwig H., Reif I., Blencke H. M., Detsch C., Stülke J. 2003; The regulatory link between carbon and nitrogen metabolism in Bacillus subtilis : regulation of the gltAB operon by the catabolite control protein CcpA. Microbiology 149:3001–3009 [CrossRef]
     [Google Scholar]
  48. Warner J. B., Lolkema J. S. 2002; Growth of Bacillus subtilis on citrate and isocitrate is supported by the Mg2+–citrate transporter CitM. Microbiology 148:3405–3412
     [Google Scholar]
  49. Warner J. B., Lolkema J. S. 2003; CcpA-dependent carbon catabolite repression in bacteria. Microbiol Mol Biol Rev 67:475–490 [CrossRef]
     [Google Scholar]
  50. Woodcock D. M., Crowther P. J., Doherty J., Jefferson S., DeCruz E., Noyer-Weidner M., Smith S. S., Michael M. Z., Graham M. W. 1989; Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17:3469–3478 [CrossRef]
     [Google Scholar]
  51. Zalieckas J. M., Wray L. V., Ferson A. E., Fisher S. H Jr. 1998; Transcription-repair coupling factor is involved in carbon catabolite repression of the Bacillus subtilis hut and gnt operons. Mol Microbiol 27:1031–1038 [CrossRef]
     [Google Scholar]
  52. Zamboni N., Fischer E., Laudert D., Aymerich S., Hohmann H. P., Sauer U. 2004; The Bacillus subtilis yqjI gene encodes the NADP+-dependent 6-P-gluconate dehydrogenase in the pentose phosphate pathway. J Bacteriol 186:4528–4534 [CrossRef]
     [Google Scholar]
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YvcK of Bacillus subtilis is required for a normal cell shape and for growth on Krebs cycle intermediates and substrates of the pentose phosphate pathway
Microbiology 151, 3777 (2005); https://doi.org/10.1099/mic.0.28172-0
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