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. 1996 Mar;178(5):1374–1385. doi: 10.1128/jb.178.5.1374-1385.1996

Regulators of aerobic and anaerobic respiration in Bacillus subtilis.

G Sun 1, E Sharkova 1, R Chesnut 1, S Birkey 1, M F Duggan 1, A Sorokin 1, P Pujic 1, S D Ehrlich 1, F M Hulett 1
PMCID: PMC177812  PMID: 8631715

Abstract

Two Bacillus subtilis genes, designated resD and resE, encode proteins that are similar to those of two-component signal transduction systems and play a regulatory role in respiration. The overlapping resD-resE genes are transcribed during vegetative growth from a very weak promoter directly upstream of resD. They are also part of a larger operon that includes three upstream genes, resABC (formerly orfX14, -15, and -16), the expression of which is strongly induced postexponentially. ResD is required for the expression of the following genes: resA, ctaA (required for heme A synthesis), and the petCBD operon (encoding subunits of the cytochrome bf complex). The resABC genes are essential genes which encode products with similarity to cytochrome c biogenesis proteins. resD null mutations are more deleterious to the cell than those of resE. resD mutant phenotypes, directly related to respiratory function, include streptomycin resistance, lack of production of aa3 or caa3 terminal oxidases, acid accumulation when grown with glucose as a carbon source, and loss of ability to grow anaerobically on a medium containing nitrate. A resD mutation also affected sporulation, carbon source utilization, and Pho regulon regulation. The data presented here support an activation role for ResD, and to a lesser extent ResE, in global regulation of aerobic and anaerobic respiration i B.subtilis.

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Selected References

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  1. Azevedo V., Sorokin A., Ehrlich S. D., Serror P. The transcriptional organization of the Bacillus subtilis 168 chromosome region between the spoVAF and serA genetic loci. Mol Microbiol. 1993 Oct;10(2):397–405. doi: 10.1111/j.1365-2958.1993.tb02671.x. [DOI] [PubMed] [Google Scholar]
  2. Beckman D. L., Kranz R. G. Cytochromes c biogenesis in a photosynthetic bacterium requires a periplasmic thioredoxin-like protein. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2179–2183. doi: 10.1073/pnas.90.6.2179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beckman D. L., Trawick D. R., Kranz R. G. Bacterial cytochromes c biogenesis. Genes Dev. 1992 Feb;6(2):268–283. doi: 10.1101/gad.6.2.268. [DOI] [PubMed] [Google Scholar]
  4. Bisschop A., Konings W. N. Reconstitution of reduced nicotinamide adenine dinucleotide oxidase activity with menadione in membrane vesicles from the menaquinone-deficient Bacillus subtilis aro D. Relation between electron transfer and active transport. Eur J Biochem. 1976 Aug 16;67(2):357–365. doi: 10.1111/j.1432-1033.1976.tb10699.x. [DOI] [PubMed] [Google Scholar]
  5. Burbulys D., Trach K. A., Hoch J. A. Initiation of sporulation in B. subtilis is controlled by a multicomponent phosphorelay. Cell. 1991 Feb 8;64(3):545–552. doi: 10.1016/0092-8674(91)90238-t. [DOI] [PubMed] [Google Scholar]
  6. Chesnut R. S., Bookstein C., Hulett F. M. Separate promoters direct expression of phoAIII, a member of the Bacillus subtilis alkaline phosphatase multigene family, during phosphate starvation and sporulation. Mol Microbiol. 1991 Sep;5(9):2181–2190. doi: 10.1111/j.1365-2958.1991.tb02148.x. [DOI] [PubMed] [Google Scholar]
  7. Compan I., Touati D. Anaerobic activation of arcA transcription in Escherichia coli: roles of Fnr and ArcA. Mol Microbiol. 1994 Mar;11(5):955–964. doi: 10.1111/j.1365-2958.1994.tb00374.x. [DOI] [PubMed] [Google Scholar]
  8. Ebbole D. J., Zalkin H. Bacillus subtilis pur operon expression and regulation. J Bacteriol. 1989 Apr;171(4):2136–2141. doi: 10.1128/jb.171.4.2136-2141.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ferrari E., Henner D. J., Perego M., Hoch J. A. Transcription of Bacillus subtilis subtilisin and expression of subtilisin in sporulation mutants. J Bacteriol. 1988 Jan;170(1):289–295. doi: 10.1128/jb.170.1.289-295.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Glaser P., Danchin A., Kunst F., Zuber P., Nakano M. M. Identification and isolation of a gene required for nitrate assimilation and anaerobic growth of Bacillus subtilis. J Bacteriol. 1995 Feb;177(4):1112–1115. doi: 10.1128/jb.177.4.1112-1115.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gunsalus R. P. Control of electron flow in Escherichia coli: coordinated transcription of respiratory pathway genes. J Bacteriol. 1992 Nov;174(22):7069–7074. doi: 10.1128/jb.174.22.7069-7074.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hansson M., Hederstedt L. Cloning and characterization of the Bacillus subtilis hemEHY gene cluster, which encodes protoheme IX biosynthetic enzymes. J Bacteriol. 1992 Dec;174(24):8081–8093. doi: 10.1128/jb.174.24.8081-8093.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hansson M., Rutberg L., Schröder I., Hederstedt L. The Bacillus subtilis hemAXCDBL gene cluster, which encodes enzymes of the biosynthetic pathway from glutamate to uroporphyrinogen III. J Bacteriol. 1991 Apr;173(8):2590–2599. doi: 10.1128/jb.173.8.2590-2599.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Henikoff S., Henikoff J. G. Automated assembly of protein blocks for database searching. Nucleic Acids Res. 1991 Dec 11;19(23):6565–6572. doi: 10.1093/nar/19.23.6565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hulett F. M., Bookstein C., Jensen K. Evidence for two structural genes for alkaline phosphatase in Bacillus subtilis. J Bacteriol. 1990 Feb;172(2):735–740. doi: 10.1128/jb.172.2.735-740.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hulett F. M., Lee J., Shi L., Sun G., Chesnut R., Sharkova E., Duggan M. F., Kapp N. Sequential action of two-component genetic switches regulates the PHO regulon in Bacillus subtilis. J Bacteriol. 1994 Mar;176(5):1348–1358. doi: 10.1128/jb.176.5.1348-1358.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Inoue T., Cech T. R. Secondary structure of the circular form of the Tetrahymena rRNA intervening sequence: a technique for RNA structure analysis using chemical probes and reverse transcriptase. Proc Natl Acad Sci U S A. 1985 Feb;82(3):648–652. doi: 10.1073/pnas.82.3.648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Iuchi S., Chepuri V., Fu H. A., Gennis R. B., Lin E. C. Requirement for terminal cytochromes in generation of the aerobic signal for the arc regulatory system in Escherichia coli: study utilizing deletions and lac fusions of cyo and cyd. J Bacteriol. 1990 Oct;172(10):6020–6025. doi: 10.1128/jb.172.10.6020-6025.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Iuchi S., Lin E. C. Adaptation of Escherichia coli to redox environments by gene expression. Mol Microbiol. 1993 Jul;9(1):9–15. doi: 10.1111/j.1365-2958.1993.tb01664.x. [DOI] [PubMed] [Google Scholar]
  20. Jensen K. K., Sharkova E., Duggan M. F., Qi Y., Koide A., Hoch J. A., Hulett F. M. Bacillus subtilis transcription regulator, Spo0A, decreases alkaline phosphatase levels induced by phosphate starvation. J Bacteriol. 1993 Jun;175(12):3749–3756. doi: 10.1128/jb.175.12.3749-3756.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kirsch M. L., Peters P. D., Hanlon D. W., Kirby J. R., Ordal G. W. Chemotactic methylesterase promotes adaptation to high concentrations of attractant in Bacillus subtilis. J Biol Chem. 1993 Sep 5;268(25):18610–18616. [PubMed] [Google Scholar]
  22. Lauraeus M., Haltia T., Saraste M., Wikström M. Bacillus subtilis expresses two kinds of haem-A-containing terminal oxidases. Eur J Biochem. 1991 May 8;197(3):699–705. doi: 10.1111/j.1432-1033.1991.tb15961.x. [DOI] [PubMed] [Google Scholar]
  23. Leighton T. J., Doi R. H. The stability of messenger ribonucleic acid during sporulation in Bacillus subtilis. J Biol Chem. 1971 May 25;246(10):3189–3195. [PubMed] [Google Scholar]
  24. Loferer H., Bott M., Hennecke H. Bradyrhizobium japonicum TlpA, a novel membrane-anchored thioredoxin-like protein involved in the biogenesis of cytochrome aa3 and development of symbiosis. EMBO J. 1993 Sep;12(9):3373–3383. doi: 10.1002/j.1460-2075.1993.tb06011.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lukat G. S., McCleary W. R., Stock A. M., Stock J. B. Phosphorylation of bacterial response regulator proteins by low molecular weight phospho-donors. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):718–722. doi: 10.1073/pnas.89.2.718. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McCleary W. R., Stock J. B. Acetyl phosphate and the activation of two-component response regulators. J Biol Chem. 1994 Dec 16;269(50):31567–31572. [PubMed] [Google Scholar]
  27. Msadek T., Kunst F., Henner D., Klier A., Rapoport G., Dedonder R. Signal transduction pathway controlling synthesis of a class of degradative enzymes in Bacillus subtilis: expression of the regulatory genes and analysis of mutations in degS and degU. J Bacteriol. 1990 Feb;172(2):824–834. doi: 10.1128/jb.172.2.824-834.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mueller J. P., Taber H. W. Isolation and sequence of ctaA, a gene required for cytochrome aa3 biosynthesis and sporulation in Bacillus subtilis. J Bacteriol. 1989 Sep;171(9):4967–4978. doi: 10.1128/jb.171.9.4967-4978.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mueller J. P., Taber H. W. Structure and expression of the cytochrome aa3 regulatory gene ctaA of Bacillus subtilis. J Bacteriol. 1989 Sep;171(9):4979–4986. doi: 10.1128/jb.171.9.4979-4986.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nakano M. M., Yang F., Hardin P., Zuber P. Nitrogen regulation of nasA and the nasB operon, which encode genes required for nitrate assimilation in Bacillus subtilis. J Bacteriol. 1995 Feb;177(3):573–579. doi: 10.1128/jb.177.3.573-579.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ogawa K., Akagawa E., Yamane K., Sun Z. W., LaCelle M., Zuber P., Nakano M. M. The nasB operon and nasA gene are required for nitrate/nitrite assimilation in Bacillus subtilis. J Bacteriol. 1995 Mar;177(5):1409–1413. doi: 10.1128/jb.177.5.1409-1413.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Petricek M., Rutberg L., Schröder I., Hederstedt L. Cloning and characterization of the hemA region of the Bacillus subtilis chromosome. J Bacteriol. 1990 May;172(5):2250–2258. doi: 10.1128/jb.172.5.2250-2258.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Santana M., Kunst F., Hullo M. F., Rapoport G., Danchin A., Glaser P. Molecular cloning, sequencing, and physiological characterization of the qox operon from Bacillus subtilis encoding the aa3-600 quinol oxidase. J Biol Chem. 1992 May 25;267(15):10225–10231. [PubMed] [Google Scholar]
  34. Saraste M., Metso T., Nakari T., Jalli T., Lauraeus M., Van der Oost J. The Bacillus subtilis cytochrome-c oxidase. Variations on a conserved protein theme. Eur J Biochem. 1991 Jan 30;195(2):517–525. doi: 10.1111/j.1432-1033.1991.tb15732.x. [DOI] [PubMed] [Google Scholar]
  35. Schröder I., Wolin C. D., Cavicchioli R., Gunsalus R. P. Phosphorylation and dephosphorylation of the NarQ, NarX, and NarL proteins of the nitrate-dependent two-component regulatory system of Escherichia coli. J Bacteriol. 1994 Aug;176(16):4985–4992. doi: 10.1128/jb.176.16.4985-4992.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Seki T., Yoshikawa H., Takahashi H., Saito H. Cloning and nucleotide sequence of phoP, the regulatory gene for alkaline phosphatase and phosphodiesterase in Bacillus subtilis. J Bacteriol. 1987 Jul;169(7):2913–2916. doi: 10.1128/jb.169.7.2913-2916.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Seki T., Yoshikawa H., Takahashi H., Saito H. Nucleotide sequence of the Bacillus subtilis phoR gene. J Bacteriol. 1988 Dec;170(12):5935–5938. doi: 10.1128/jb.170.12.5935-5938.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Shimotsu H., Henner D. J. Construction of a single-copy integration vector and its use in analysis of regulation of the trp operon of Bacillus subtilis. Gene. 1986;43(1-2):85–94. doi: 10.1016/0378-1119(86)90011-9. [DOI] [PubMed] [Google Scholar]
  39. Sorokin A., Zumstein E., Azevedo V., Ehrlich S. D., Serror P. The organization of the Bacillus subtilis 168 chromosome region between the spoVA and serA genetic loci, based on sequence data. Mol Microbiol. 1993 Oct;10(2):385–395. doi: 10.1111/j.1365-2958.1993.tb02670.x. [DOI] [PubMed] [Google Scholar]
  40. Spiro S., Guest J. R. Adaptive responses to oxygen limitation in Escherichia coli. Trends Biochem Sci. 1991 Aug;16(8):310–314. doi: 10.1016/0968-0004(91)90125-f. [DOI] [PubMed] [Google Scholar]
  41. Spizizen J. TRANSFORMATION OF BIOCHEMICALLY DEFICIENT STRAINS OF BACILLUS SUBTILIS BY DEOXYRIBONUCLEATE. Proc Natl Acad Sci U S A. 1958 Oct 15;44(10):1072–1078. doi: 10.1073/pnas.44.10.1072. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Staal S. P., Hoch J. A. Conditional dihydrostreptomycin resistance in Bacillus subtilis. J Bacteriol. 1972 Apr;110(1):202–207. doi: 10.1128/jb.110.1.202-207.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Stewart V. Nitrate regulation of anaerobic respiratory gene expression in Escherichia coli. Mol Microbiol. 1993 Aug;9(3):425–434. doi: 10.1111/j.1365-2958.1993.tb01704.x. [DOI] [PubMed] [Google Scholar]
  44. Svensson B., Hederstedt L. Bacillus subtilis CtaA is a heme-containing membrane protein involved in heme A biosynthesis. J Bacteriol. 1994 Nov;176(21):6663–6671. doi: 10.1128/jb.176.21.6663-6671.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Svensson B., Lübben M., Hederstedt L. Bacillus subtilis CtaA and CtaB function in haem A biosynthesis. Mol Microbiol. 1993 Oct;10(1):193–201. doi: 10.1111/j.1365-2958.1993.tb00915.x. [DOI] [PubMed] [Google Scholar]
  46. Thöny-Meyer L., Ritz D., Hennecke H. Cytochrome c biogenesis in bacteria: a possible pathway begins to emerge. Mol Microbiol. 1994 Apr;12(1):1–9. doi: 10.1111/j.1365-2958.1994.tb00988.x. [DOI] [PubMed] [Google Scholar]
  47. Trumpower B. L. Cytochrome bc1 complexes of microorganisms. Microbiol Rev. 1990 Jun;54(2):101–129. doi: 10.1128/mr.54.2.101-129.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Trumpower B. L., Gennis R. B. Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration: the enzymology of coupling electron transfer reactions to transmembrane proton translocation. Annu Rev Biochem. 1994;63:675–716. doi: 10.1146/annurev.bi.63.070194.003331. [DOI] [PubMed] [Google Scholar]

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