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. 1993 Nov;175(22):7200–7208. doi: 10.1128/jb.175.22.7200-7208.1993

Two global regulatory systems (Crp and Arc) control the cobalamin/propanediol regulon of Salmonella typhimurium.

M Ailion 1, T A Bobik 1, J R Roth 1
PMCID: PMC206861  PMID: 8226666

Abstract

The genes for cobalamin (vitamin B12) biosynthesis (cob) are coregulated with genes for degradation of propanediol (pdu). Both the cob and pdu operons are induced by propanediol by means of a positive regulatory protein, PocR. This coregulation of a synthetic and a degradative pathway reflects the fact that vitamin B12 is a required cofactor for the first enzyme in propanediol breakdown. The cob/pdu regulon is induced by propanediol under two sets of growth conditions, i.e., during aerobic respiration of a poor carbon source and during anaerobic growth. We provide evidence that, under aerobic conditions, the Crp/cyclic AMP system is needed for all induction of the pocR, cob, and pdu genes. Anaerobically, the Crp/cyclic AMP and ArcA/ArcB systems act additively to support induction of the same three transcription units. The fact that these global control systems affect expression of the gene for the positive regulatory protein (pocR) as well as the pdu and cob operons is consistent with our previous suggestion that these two global controls may act directly only on the pocR gene; their control over the cob and pdu operons may be an indirect consequence of their effect on the level of PocR activator protein. The reported experiments were made possible by the observation that pyruvate supports aerobic growth of all of the mutants tested (cya, crp, arcA, and arcB); pyruvate also supports anaerobic growth of these mutants if the alternative electron acceptor, fumarate, is provided. By using pyruvate as a carbon source, it was possible to grow all of these mutant strains under identical conditions and compare their expression of the cob/pdu regulon. The role of Crp in control of vitamin B12 synthesis suggests that the major role of vitamin B12 in Salmonella spp. is in catabolism of carbon sources; the coregulation of the cob and pdu operons suggests that propanediol is the major vitamin B12-dependent carbon source.

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Selected References

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  1. Andersson D. I. Involvement of the Arc system in redox regulation of the Cob operon in Salmonella typhimurium. Mol Microbiol. 1992 Jun;6(11):1491–1494. doi: 10.1111/j.1365-2958.1992.tb00869.x. [DOI] [PubMed] [Google Scholar]
  2. Andersson D. I., Roth J. R. Mutations affecting regulation of cobinamide biosynthesis in Salmonella typhimurium. J Bacteriol. 1989 Dec;171(12):6726–6733. doi: 10.1128/jb.171.12.6726-6733.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Andersson D. I., Roth J. R. Redox regulation of the genes for cobinamide biosynthesis in Salmonella typhimurium. J Bacteriol. 1989 Dec;171(12):6734–6739. doi: 10.1128/jb.171.12.6734-6739.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berkowitz D., Hushon J. M., Whitfield H. J., Jr, Roth J., Ames B. N. Procedure for identifying nonsense mutations. J Bacteriol. 1968 Jul;96(1):215–220. doi: 10.1128/jb.96.1.215-220.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bobik T. A., Ailion M., Roth J. R. A single regulatory gene integrates control of vitamin B12 synthesis and propanediol degradation. J Bacteriol. 1992 Apr;174(7):2253–2266. doi: 10.1128/jb.174.7.2253-2266.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Botsford J. L., Harman J. G. Cyclic AMP in prokaryotes. Microbiol Rev. 1992 Mar;56(1):100–122. doi: 10.1128/mr.56.1.100-122.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Casadaban M. J., Cohen S. N. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530–4533. doi: 10.1073/pnas.76.9.4530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. 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]
  10. Cotter P. A., Gunsalus R. P. Contribution of the fnr and arcA gene products in coordinate regulation of cytochrome o and d oxidase (cyoABCDE and cydAB) genes in Escherichia coli. FEMS Microbiol Lett. 1992 Feb 1;70(1):31–36. doi: 10.1016/0378-1097(92)90558-6. [DOI] [PubMed] [Google Scholar]
  11. Elliott T., Roth J. R. Characterization of Tn10d-Cam: a transposition-defective Tn10 specifying chloramphenicol resistance. Mol Gen Genet. 1988 Aug;213(2-3):332–338. doi: 10.1007/BF00339599. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Fu H. A., Iuchi S., Lin E. C. The requirement of ArcA and Fnr for peak expression of the cyd operon in Escherichia coli under microaerobic conditions. Mol Gen Genet. 1991 Apr;226(1-2):209–213. doi: 10.1007/BF00273605. [DOI] [PubMed] [Google Scholar]
  14. Hughes K. T., Roth J. R. Conditionally transposition-defective derivative of Mu d1(Amp Lac). J Bacteriol. 1984 Jul;159(1):130–137. doi: 10.1128/jb.159.1.130-137.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Iuchi S., Cameron D. C., Lin E. C. A second global regulator gene (arcB) mediating repression of enzymes in aerobic pathways of Escherichia coli. J Bacteriol. 1989 Feb;171(2):868–873. doi: 10.1128/jb.171.2.868-873.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Iuchi S., Lin E. C. arcA (dye), a global regulatory gene in Escherichia coli mediating repression of enzymes in aerobic pathways. Proc Natl Acad Sci U S A. 1988 Mar;85(6):1888–1892. doi: 10.1073/pnas.85.6.1888. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jeter R. M. Cobalamin-dependent 1,2-propanediol utilization by Salmonella typhimurium. J Gen Microbiol. 1990 May;136(5):887–896. doi: 10.1099/00221287-136-5-887. [DOI] [PubMed] [Google Scholar]
  18. Jeter R. M., Olivera B. M., Roth J. R. Salmonella typhimurium synthesizes cobalamin (vitamin B12) de novo under anaerobic growth conditions. J Bacteriol. 1984 Jul;159(1):206–213. doi: 10.1128/jb.159.1.206-213.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jeter R. M., Roth J. R. Cobalamin (vitamin B12) biosynthetic genes of Salmonella typhimurium. J Bacteriol. 1987 Jul;169(7):3189–3198. doi: 10.1128/jb.169.7.3189-3198.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kleckner N., Bender J., Gottesman S. Uses of transposons with emphasis on Tn10. Methods Enzymol. 1991;204:139–180. doi: 10.1016/0076-6879(91)04009-d. [DOI] [PubMed] [Google Scholar]
  21. Rondon M. R., Escalante-Semerena J. C. The poc locus is required for 1,2-propanediol-dependent transcription of the cobalamin biosynthetic (cob) and propanediol utilization (pdu) genes of Salmonella typhimurium. J Bacteriol. 1992 Apr;174(7):2267–2272. doi: 10.1128/jb.174.7.2267-2272.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Roof D. M., Roth J. R. Ethanolamine utilization in Salmonella typhimurium. J Bacteriol. 1988 Sep;170(9):3855–3863. doi: 10.1128/jb.170.9.3855-3863.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Roth J. R., Lawrence J. G., Rubenfield M., Kieffer-Higgins S., Church G. M. Characterization of the cobalamin (vitamin B12) biosynthetic genes of Salmonella typhimurium. J Bacteriol. 1993 Jun;175(11):3303–3316. doi: 10.1128/jb.175.11.3303-3316.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Savage D. C. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol. 1977;31:107–133. doi: 10.1146/annurev.mi.31.100177.000543. [DOI] [PubMed] [Google Scholar]
  25. Schmieger H. A method for detection of phage mutants with altered transducing ability. Mol Gen Genet. 1971;110(4):378–381. doi: 10.1007/BF00438281. [DOI] [PubMed] [Google Scholar]
  26. Toraya T., Honda S., Fukui S. Fermentation of 1,2-propanediol with 1,2-ethanediol by some genera of Enterobacteriaceae, involving coenzyme B12-dependent diol dehydratase. J Bacteriol. 1979 Jul;139(1):39–47. doi: 10.1128/jb.139.1.39-47.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. VOGEL H. J., BONNER D. M. Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956 Jan;218(1):97–106. [PubMed] [Google Scholar]
  28. Way J. C., Davis M. A., Morisato D., Roberts D. E., Kleckner N. New Tn10 derivatives for transposon mutagenesis and for construction of lacZ operon fusions by transposition. Gene. 1984 Dec;32(3):369–379. doi: 10.1016/0378-1119(84)90012-x. [DOI] [PubMed] [Google Scholar]

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