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. 1988 Feb;170(2):842–851. doi: 10.1128/jb.170.2.842-851.1988

Novel regulatory loci controlling oxygen- and pH-regulated gene expression in Salmonella typhimurium.

Z Aliabadi 1, Y K Park 1, J L Slonczewski 1, J W Foster 1
PMCID: PMC210731  PMID: 3276666

Abstract

Three new loci were discovered, each of which participates in the regulation of anaerobic gene expression. The regulatory gene earA negatively regulates the expression of the anaerobiosis-inducible gene aniG as well as that of at least three other genes, as determined by two-dimensional polyacrylamide gel electrophoresis. The earA locus maps at 86 min. The expression of aniG was also shown to be controlled by changes in external pH under aerobic and anaerobic conditions. Maximal expression was observed under anaerobic conditions at an external pH of 6.0. Significant transcriptional activity was also observed under aerobic conditions at pH 6.0. This was in contrast to hyd, whose expression was dependent upon anaerobiosis and varied with external pH. The pH dependence disappeared under fully aerobic conditions. Mutations in earA had no effect upon hyd expression. The two other regulators identified were oxrF, which controls aniH, and oxrG, which, in concert with oxrA and oxrB, controls aniC and aniI. The oxrG locus was mapped to 88 min and appears to code for a positive regulator. Various oxr mutants were subjected to two-dimensional polyacrylamide electrophoretic analysis of anaerobiosis-inducible proteins. Several pathways of anaerobic control were observed by means of these techniques.

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Selected References

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  1. Aliabadi Z., Warren F., Mya S., Foster J. W. Oxygen-regulated stimulons of Salmonella typhimurium identified by Mu d(Ap lac) operon fusions. J Bacteriol. 1986 Mar;165(3):780–786. doi: 10.1128/jb.165.3.780-786.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barrett E. L., Jackson C. E., Fukumoto H. T., Chang G. W. Formate dehydrogenase mutants of Salmonella typhimurium: a new medium for their isolation and new mutant classes. Mol Gen Genet. 1979;177(1):95–101. doi: 10.1007/BF00267258. [DOI] [PubMed] [Google Scholar]
  3. Bilous P. T., Weiner J. H. Dimethyl sulfoxide reductase activity by anaerobically grown Escherichia coli HB101. J Bacteriol. 1985 Jun;162(3):1151–1155. doi: 10.1128/jb.162.3.1151-1155.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bonnefoy V., Pascal M. C., Ratouchniak J., Chippaux M. Alteration by mutation of the control by oxygen of the nar operon in Escherichia coli. Mol Gen Genet. 1986 Nov;205(2):349–352. doi: 10.1007/BF00430449. [DOI] [PubMed] [Google Scholar]
  5. Castilho B. A., Olfson P., Casadaban M. J. Plasmid insertion mutagenesis and lac gene fusion with mini-mu bacteriophage transposons. J Bacteriol. 1984 May;158(2):488–495. doi: 10.1128/jb.158.2.488-495.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chan R. K., Botstein D., Watanabe T., Ogata Y. Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium. II. Properties of a high-frequency-transducing lysate. Virology. 1972 Dec;50(3):883–898. doi: 10.1016/0042-6822(72)90442-4. [DOI] [PubMed] [Google Scholar]
  7. Chippaux M., Bonnefoy-Orth V., Ratouchniak J., Pascal M. C. Operon fusions in the nitrate reductase operon and study of the control gene nir R in Escherichia coli. Mol Gen Genet. 1981;182(3):477–479. doi: 10.1007/BF00293938. [DOI] [PubMed] [Google Scholar]
  8. Christman M. F., Morgan R. W., Jacobson F. S., Ames B. N. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium. Cell. 1985 Jul;41(3):753–762. doi: 10.1016/s0092-8674(85)80056-8. [DOI] [PubMed] [Google Scholar]
  9. Chumley F. G., Menzel R., Roth J. R. Hfr formation directed by tn10. Genetics. 1979 Apr;91(4):639–655. doi: 10.1093/genetics/91.4.639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Clark M. A., Barrett E. L. The phs gene and hydrogen sulfide production by Salmonella typhimurium. J Bacteriol. 1987 Jun;169(6):2391–2397. doi: 10.1128/jb.169.6.2391-2397.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Escalante-Semerena J. C., Roth J. R. Regulation of cobalamin biosynthetic operons in Salmonella typhimurium. J Bacteriol. 1987 May;169(5):2251–2258. doi: 10.1128/jb.169.5.2251-2258.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fimmel A. L., Haddock B. A. Use of chlC-lac fusions to determine regulation of gene chlC in Escherichia coli K-12. J Bacteriol. 1979 Jun;138(3):726–730. doi: 10.1128/jb.138.3.726-730.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gharbi S., Belaich A., Murgier M., Lazdunski A. Multiple controls exerted on in vivo expression of the pepN gene in Escherichia coli: studies with pepN-lacZ operon and protein fusion strains. J Bacteriol. 1985 Sep;163(3):1191–1195. doi: 10.1128/jb.163.3.1191-1195.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Holley E. A., Foster J. W. Bacteriophage P22 as a vector for Mu mutagenesis in Salmonella typhimurium: isolation of nad-lac and pnc-lac gene fusions. J Bacteriol. 1982 Nov;152(2):959–962. doi: 10.1128/jb.152.2.959-962.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Holley E. A., Spector M. P., Foster J. W. Regulation of NAD biosynthesis in Salmonella typhimurium: expression of nad-lac gene fusions and identification of a nad regulatory locus. J Gen Microbiol. 1985 Oct;131(10):2759–2770. doi: 10.1099/00221287-131-10-2759. [DOI] [PubMed] [Google Scholar]
  16. Jamieson D. J., Higgins C. F. Anaerobic and leucine-dependent expression of a peptide transport gene in Salmonella typhimurium. J Bacteriol. 1984 Oct;160(1):131–136. doi: 10.1128/jb.160.1.131-136.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jamieson D. J., Higgins C. F. Two genetically distinct pathways for transcriptional regulation of anaerobic gene expression in Salmonella typhimurium. J Bacteriol. 1986 Oct;168(1):389–397. doi: 10.1128/jb.168.1.389-397.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Jamieson D. J., Sawers R. G., Rugman P. A., Boxer D. H., Higgins C. F. Effects of anaerobic regulatory mutations and catabolite repression on regulation of hydrogen metabolism and hydrogenase isoenzyme composition in Salmonella typhimurium. J Bacteriol. 1986 Oct;168(1):405–411. doi: 10.1128/jb.168.1.405-411.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jones H. M., Gunsalus R. P. Regulation of Escherichia coli fumarate reductase (frdABCD) operon expression by respiratory electron acceptors and the fnr gene product. J Bacteriol. 1987 Jul;169(7):3340–3349. doi: 10.1128/jb.169.7.3340-3349.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jones H. M., Gunsalus R. P. Transcription of the Escherichia coli fumarate reductase genes (frdABCD) and their coordinate regulation by oxygen, nitrate, and fumarate. J Bacteriol. 1985 Dec;164(3):1100–1109. doi: 10.1128/jb.164.3.1100-1109.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Kuritzkes D. R., Zhang X. Y., Lin E. C. Use of phi(glp-lac) in studies of respiratory regulation of the Escherichia coli anaerobic sn-glycerol-3-phosphate dehydrogenase genes (glpAB). J Bacteriol. 1984 Feb;157(2):591–598. doi: 10.1128/jb.157.2.591-598.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kwan H. S., Barrett E. L. Roles for menaquinone and the two trimethylamine oxide (TMAO) reductases in TMAO respiration in Salmonella typhimurium: Mu d(Apr lac) insertion mutations in men and tor. J Bacteriol. 1983 Sep;155(3):1147–1155. doi: 10.1128/jb.155.3.1147-1155.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lambden P. R., Guest J. R. Mutants of Escherichia coli K12 unable to use fumarate as an anaerobic electron acceptor. J Gen Microbiol. 1976 Dec;97(2):145–160. doi: 10.1099/00221287-97-2-145. [DOI] [PubMed] [Google Scholar]
  24. Maloy S. R., Nunn W. D. Selection for loss of tetracycline resistance by Escherichia coli. J Bacteriol. 1981 Feb;145(2):1110–1111. doi: 10.1128/jb.145.2.1110-1111.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Merberg D., Datta P. Altered expression of biodegradative threonine dehydratase in Escherichia coli mutants. J Bacteriol. 1982 Apr;150(1):52–59. doi: 10.1128/jb.150.1.52-59.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Neidhardt F. C., Bloch P. L., Smith D. F. Culture medium for enterobacteria. J Bacteriol. 1974 Sep;119(3):736–747. doi: 10.1128/jb.119.3.736-747.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pascal M. C., Burini J. F., Chippaux M. Regulation of the trimethylamine N-oxide (TMAO) reductase in Escherichia coli: analysis of tor::Mud1 operon fusion. Mol Gen Genet. 1984;195(1-2):351–355. doi: 10.1007/BF00332770. [DOI] [PubMed] [Google Scholar]
  28. Pecher A., Zinoni F., Jatisatienr C., Wirth R., Hennecke H., Böck A. On the redox control of synthesis of anaerobically induced enzymes in enterobacteriaceae. Arch Microbiol. 1983 Nov;136(2):131–136. doi: 10.1007/BF00404787. [DOI] [PubMed] [Google Scholar]
  29. Slonczewski J. L., Gonzalez T. N., Bartholomew F. M., Holt N. J. Mu d-directed lacZ fusions regulated by low pH in Escherichia coli. J Bacteriol. 1987 Jul;169(7):3001–3006. doi: 10.1128/jb.169.7.3001-3006.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Spector M. P., Aliabadi Z., Gonzalez T., Foster J. W. Global control in Salmonella typhimurium: two-dimensional electrophoretic analysis of starvation-, anaerobiosis-, and heat shock-inducible proteins. J Bacteriol. 1986 Oct;168(1):420–424. doi: 10.1128/jb.168.1.420-424.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Stewart V. Requirement of Fnr and NarL functions for nitrate reductase expression in Escherichia coli K-12. J Bacteriol. 1982 Sep;151(3):1320–1325. doi: 10.1128/jb.151.3.1320-1325.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Strauch K. L., Lenk J. B., Gamble B. L., Miller C. G. Oxygen regulation in Salmonella typhimurium. J Bacteriol. 1985 Feb;161(2):673–680. doi: 10.1128/jb.161.2.673-680.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Winkelman J. W., Clark D. P. Anaerobically induced genes of Escherichia coli. J Bacteriol. 1986 Jul;167(1):362–367. doi: 10.1128/jb.167.1.362-367.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Yamamoto N., Droffner M. L. Mechanisms determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. Proc Natl Acad Sci U S A. 1985 Apr;82(7):2077–2081. doi: 10.1073/pnas.82.7.2077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Zinoni F., Beier A., Pecher A., Wirth R., Böck A. Regulation of the synthesis of hydrogenase (formate hydrogen-lyase linked) of E. coli. Arch Microbiol. 1984 Nov;139(4):299–304. doi: 10.1007/BF00408370. [DOI] [PubMed] [Google Scholar]

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