1887

Abstract

A variety of pathways for electron and carbon flow in the soil bacterium are differentially expressed depending on whether oxygen is present in the cell environment. This study characterizes the regulation of the respiratory oxidase cytochrome and the NADH-linked fermentative lactate dehydrogenase (LDH). Transcription of the operon, encoding cytochrome , is highly regulated and only becomes activated at low oxygen availability. This induction is not dependent on the gene encoding the redox regulator Fnr or the genes encoding the ResDE two-component regulatory system. The DNA-binding protein YdiH was found to be a principal regulator that controls expression. Transcription from the promoter is stimulated 15-fold by a region located upstream of the core promoter. The upstream region may constitute a binding site for an unidentified transcription activator that is likely to influence the level of transcription but not its timing, which is negatively controlled by YdiH. This report provides evidence that YdiH also functions as a repressor of the gene encoding LDH and of a gene, , which encodes a putative formate-nitrite transporter. Based on the similarity between YdiH and the Rex protein of , it is proposed that YdiH serves as a redox sensor, the activity of which is regulated by cellular differences in the free levels of NAD and NADH. It is suggested that be renamed as .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28124-0
2005-10-01
2019-11-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/10/3323.html?itemId=/content/journal/micro/10.1099/mic.0.28124-0&mimeType=html&fmt=ahah

References

  1. Arras, T., Schirawski, J. & Unden, G. ( 1998; ). Availability of O2 as a substrate in the cytoplasm of bacteria under aerobic and microaerobic conditions. J Bacteriol 180, 2133–2136.
    [Google Scholar]
  2. Brekasis, D. & Paget, M. S. ( 2003; ). A novel sensor of NADH/NAD+ redox poise in Streptomyces coelicolor A3(2). EMBO J 22, 4856–4865.[CrossRef]
    [Google Scholar]
  3. Brigulla, M., Hoffmann, T., Krisp, A., Völker, A., Bremer, E. & Völker, U. ( 2003; ). Chill induction of the SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. J Bacteriol 185, 4305–4314.[CrossRef]
    [Google Scholar]
  4. Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. ( 2004; ). weblogo: a sequence logo generator. Genome Res 14, 1188–1190.[CrossRef]
    [Google Scholar]
  5. Cruz Ramos, H., Boursier, L., Moszer, I., Kunst, F., Danchin, A. & Glaser, P. ( 1995; ). Anaerobic transcription activation in Bacillus subtilis: identification of distinct FNR-dependent and -independent regulatory mechanisms. EMBO J 14, 5984–5994.
    [Google Scholar]
  6. Cruz Ramos, H., Hoffmann, T., Marino, M., Nedjari, H., Presecan-Siedel, E., Dreesen, O., Glaser, P. & Jahn, D. ( 2000; ). Fermentative metabolism of Bacillus subtilis: physiology and regulation of gene expression. J Bacteriol 182, 3072–3080.[CrossRef]
    [Google Scholar]
  7. Geng, H., Nakano, S. & Nakano, M. M. ( 2004; ). Transcriptional activation by Bacillus subtilis ResD: tandem binding to target elements and phosphorylation-dependent and -independent transcriptional activation. J Bacteriol 186, 2028–2037.[CrossRef]
    [Google Scholar]
  8. Gennis, R. B. & Stewart, V. ( 1996; ). Respiration. In Escherichia coli and Salmonella: Cellular and Molecular Biology, pp. 217–261. Edited by F. C. Neidhart. Washington, DC: American Society for Microbiology.
  9. Giangiacomo, L., Ilari, A., Boffi, A., Morea, V. & Chiancone, E. ( 2005; ). The truncated oxygen-avid hemoglobin from Bacillus subtilis: X-ray structure and ligand binding properties. J Biol Chem 280, 9192–9202.[CrossRef]
    [Google Scholar]
  10. Glaser, P., Kunst, F., Arnaud, M. & 14 other authors ( 1993; ). Bacillus subtilis genome project: cloning and sequencing of the 97 kb region from 325 degrees to 333 degrees. Mol Microbiol 10, 371–384.[CrossRef]
    [Google Scholar]
  11. Green, J. & Paget, M. S. ( 2004; ). Bacterial redox sensors. Nat Rev Microbiol 2, 954–966.[CrossRef]
    [Google Scholar]
  12. Guerout-Fleury, A. M., Frandsen, N. & Stragier, P. ( 1996; ). Plasmids for ectopic integration in Bacillus subtilis. Gene 180, 57–61.[CrossRef]
    [Google Scholar]
  13. Hecker, M. & Völker, U. ( 2001; ). General stress response of Bacillus subtilis and other bacteria. Adv Microb Physiol 44, 35–91.
    [Google Scholar]
  14. Hederstedt, L. ( 1986; ). Molecular properties, genetics, and biosynthesis of Bacillus subtilis succinate dehydrogenase complex. Methods Enzymol 126, 399–414.
    [Google Scholar]
  15. Hoch, J. A. ( 1991; ). Genetic analysis in Bacillus subtilis. Methods Enzymol 204, 305–320.
    [Google Scholar]
  16. Holmberg, C. & Rutberg, L. ( 1992; ). An inverted repeat preceding the Bacillus subtilis glpD gene is a conditional terminator of transcription. Mol Microbiol 6, 2931–2938.[CrossRef]
    [Google Scholar]
  17. Jarmer, H., Larsen, T. S., Krogh, A., Saxild, H. H., Brunak, S. & Knudsen, S. ( 2001; ). Sigma A recognition sites in the Bacillus subtilis genome. Microbiology 147, 2417–2424.
    [Google Scholar]
  18. Jünemann, S. ( 1997; ). Cytochrome bd terminal oxidase. Biochim Biophys Acta 1321, 107–127.[CrossRef]
    [Google Scholar]
  19. Korner, H., Sofia, H. J. & Zumft, W. G. ( 2003; ). Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 27, 559–592.[CrossRef]
    [Google Scholar]
  20. Kruger, S., Stülke, J. & Hecker, M. ( 1993; ). Catabolite repression of beta-glucanase synthesis in Bacillus subtilis. J Gen Microbiol 139, 2047–2054.[CrossRef]
    [Google Scholar]
  21. Makita, Y., Nakao, M., Ogasawara, N. & Nakai, K. ( 2004; ). dbtbs: database of transcriptional regulation in Bacillus subtilis and its contribution to comparative genomics. Nucleic Acids Res 32 (database issue), D75–D77.[CrossRef]
    [Google Scholar]
  22. Marino, M., Hoffmann, T., Schmid, R., Mobitz, H. & Jahn, D. ( 2000; ). Changes in protein synthesis during the adaptation of Bacillus subtilis to anaerobic growth conditions. Microbiology 146, 97–105.
    [Google Scholar]
  23. Moreno, M. S., Schneider, B. L., Maile, R. R., Weyler, W. & Saier, M. H. ( 2001; ). Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol Microbiol 39, 1366–1381.[CrossRef]
    [Google Scholar]
  24. Nakano, M. M. & Zuber, P. ( 2002; ). Anaerobiosis. In Bacillus subtilis and its Closest Relatives: from Genes to Cells, pp. 393–404. Edited by A. L. Sonenshein, J. A. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
    [Google Scholar]
  25. Nakano, M. M., Zhu, Y., Lacelle, M., Zhang, X. & Hulett, F. M. ( 2000; ). Interaction of ResD with regulatory regions of anaerobically induced genes in Bacillus subtilis. Mol Microbiol 37, 1198–1207.[CrossRef]
    [Google Scholar]
  26. Petersohn, A., Brigulla, M., Haas, S., Hoheisel, J. D., Völker, U. & Hecker, M. ( 2001; ). Global analysis of the general stress response of Bacillus subtilis. J Bacteriol 183, 5617–5631.[CrossRef]
    [Google Scholar]
  27. Poole, R. K. & Cook, G. M. ( 2000; ). Redundancy of aerobic respiratory chains in bacteria? Routes, reasons and regulation. Adv Microb Physiol 43, 165–224.
    [Google Scholar]
  28. Presecan-Siedel, E., Galinier, A., Longin, R., Deutscher, J., Danchin, A., Glaser, P. & Martin-Verstraete, I. ( 1999; ). Catabolite regulation of the pta gene as part of carbon flow pathways in Bacillus subtilis. J Bacteriol 181, 6889–6897.
    [Google Scholar]
  29. Price, C. W., Fawcett, P., Ceremonie, H., Su, N., Murphy, C. K. & Youngman, P. ( 2001; ). Genome-wide analysis of the general stress response in Bacillus subtilis. Mol Microbiol 41, 757–774.
    [Google Scholar]
  30. Saal, L. H., Troein, C., Vallon-Christersson, J., Gruvberger, S., Borg, A. & Peterson, C. ( 2002; ). BioArray Software Environment (base): a platform for comprehensive management and analysis of microarray data. Genome Biol 3, SOFTWARE0003.
    [Google Scholar]
  31. Sambrook, J. & Russel, D. W. ( 2001; ). Molecular Cloning. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  32. Schau, M., Chen, Y. & Hulett, F. M. ( 2004; ). Bacillus subtilis YdiH is a direct negative regulator of the cydABCD operon. J Bacteriol 186, 4585–4595.[CrossRef]
    [Google Scholar]
  33. Schiött, T., von Wachenfeldt, C. & Hederstedt, L. ( 1997; ). Identification and characterization of the ccdA gene, required for cytochrome c synthesis in Bacillus subtilis. J Bacteriol 179, 1962–1973.
    [Google Scholar]
  34. Sickmier, E. A., Brekasis, D., Paranawithana, S., Bonanno, J. B., Paget, M. S., Burley, S. K. & Kielkopf, C. L. ( 2005; ). X-ray structure of a Rex-family repressor/NADH complex insights into the mechanism of redox sensing. Structure 13, 43–54.[CrossRef]
    [Google Scholar]
  35. Sun, G., Sharkova, E., Chesnut, R., Birkey, S., Duggan, M. F., Sorokin, A., Pujic, P., Ehrlich, S. D. & Hulett, F. M. ( 1996; ). Regulators of aerobic and anaerobic respiration in Bacillus subtilis. J Bacteriol 178, 1374–1385.
    [Google Scholar]
  36. van Helden, J., Andre, B. & Collado-Vides, J. ( 2000; ). A web site for the computational analysis of yeast regulatory sequences. Yeast 16, 177–187.[CrossRef]
    [Google Scholar]
  37. Vijay, K., Brody, M. S., Fredlund, E. & Price, C. W. ( 2000; ). A PP2C phosphatase containing a PAS domain is required to convey signals of energy stress to the sigmaB transcription factor of Bacillus subtilis. Mol Microbiol 35, 180–188.[CrossRef]
    [Google Scholar]
  38. von Wachenfeldt, C. & Hederstedt, L. ( 2002; ). Respiratory cytochromes, other heme proteins, and heme biosynthesis. In Bacillus subtilis and its Closest Relatives: from Genes to Cells, pp. 163–179. Edited by A. L. Sonenshein, J. A. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
  39. Winstedt, L. & von Wachenfeldt, C. ( 2000; ). Terminal oxidases of Bacillus subtilis strain 168: one quinol oxidase, cytochrome aa 3 or cytochrome bd, is required for aerobic growth. J Bacteriol 182, 6557–6564.[CrossRef]
    [Google Scholar]
  40. Winstedt, L., Yoshida, K., Fujita, Y. & von Wachenfeldt, C. ( 1998; ). Cytochrome bd biosynthesis in Bacillus subtilis: characterization of the cydABCD operon. J Bacteriol 180, 6571–6580.
    [Google Scholar]
  41. Wittenberg, J. B., Bolognesi, M., Wittenberg, B. A. & Guertin, M. ( 2002; ). Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes, and plants. J Biol Chem 277, 871–874.[CrossRef]
    [Google Scholar]
  42. Yang, H., Haddad, H., Tomas, C., Alsaker, K. & Papoutsakis, E. T. ( 2003; ). A segmental nearest neighbor normalization and gene identification method gives superior results for DNA-array analysis. Proc Natl Acad Sci U S A 100, 1122–1127.[CrossRef]
    [Google Scholar]
  43. Yoshida, K., Kobayashi, K., Miwa, Y. & 9 other authors ( 2001; ). Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis. Nucleic Acids Res 29, 683–692.[CrossRef]
    [Google Scholar]
  44. Youngman, P. ( 1990; ). Use of transposons and integrational vectors for mutagenesis and construction of gene fusions in Bacillus subtilis. In Molecular Biological Methods for Bacillus, pp. 221–266. Edited by C. R. Harwood & S. M. Cutting. New York: Wiley.
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28124-0
Loading
/content/journal/micro/10.1099/mic.0.28124-0
Loading

Data & Media loading...

Supplements

link text(104 KB)

TEXT

link text(102 KB)

TEXT

link text(107 KB)

TEXT

link text(3 KB)

TEXT

link text(3 KB)

TEXT

link text(871 KB)

TEXT

Light absorption difference (dithionite reduced minus ferricyanide-oxidized) spectra of membranes [PDF file](186 KB)

PDF

Oligonucleotide sequences [PDF file](29 KB)

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error