Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Sep;177(17):4841–4850. doi: 10.1128/jb.177.17.4841-4850.1995

Suppression of the pleiotropic effects of HisH and HisF overproduction identifies four novel loci on the Salmonella typhimurium chromosome: osmH, sfiW, sfiX, and sfiY.

A Flores 1, J Casadesús 1
PMCID: PMC177256  PMID: 7665459

Abstract

Insertion mutations that suppress some or all the pleiotropic effects of HisH and HisF overproduction were obtained by using transposons Tn10dTet and Tn10dCam. All suppressor mutations proved to be recessive, indicating that their effects were caused by loss of function; thus, the suppressors identify genes that are necessary to trigger the pleiotropic response when HisH and HisF are overproduced. Genetic mapping of the suppressor mutations identifies four novel loci on the Salmonella typhimurium genetic map. Mutations in osmH (min 49) behave as general suppressors that abolish all manifestations of the pleiotropic response. Mutations in sfiY (min 83) suppress cell division inhibition and thermosensitivity but not osmosensitivity. Mutations that suppress only cell division inhibition define another locus, sfiX (min 44). A fourth novel locus, sfiW (min 19), is also involved in cell division inhibition. The phenotype of sfiW mutations is in turn pleiotropic: they suppress cell division inhibition, make S. typhimurium unable to grow in minimal media, and cause slow growth and abnormal colony and cell shape. The inability of sfiW mutants to grow in minimal medium cannot be relieved by any known nutritional requirement or by the use of carbon sources other than glucose. The hierarchy of suppressor phenotypes and the existence of epistatic effects among suppressor mutations suggest a pathway-like model for the Hisc pleiotropic response.

Full Text

The Full Text of this article is available as a PDF (804.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abstracts of papers presented at the 1980 meetings of the Genetic Society of America. Boulder, Colorado August 18-20, 1980. Genetics. 1980;94(4 Pt 2 Suppl):1–16. [PMC free article] [PubMed] [Google Scholar]
  2. Alifano P., Piscitelli C., Blasi V., Rivellini F., Nappo A. G., Bruni C. B., Carlomagno M. S. Processing of a polycistronic mRNA requires a 5' cis element and active translation. Mol Microbiol. 1992 Mar;6(6):787–798. doi: 10.1111/j.1365-2958.1992.tb01529.x. [DOI] [PubMed] [Google Scholar]
  3. Anderson R. P., Roth J. R. Gene duplication in bacteria: alteration of gene dosage by sister-chromosome exchanges. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 2):1083–1087. doi: 10.1101/sqb.1979.043.01.120. [DOI] [PubMed] [Google Scholar]
  4. Antón D. N. Positive selection of mutants with cell envelope defects of a Salmonells typhimurium strain hypersensitive to the products of genes hisF and hisH. J Bacteriol. 1979 Mar;137(3):1271–1281. doi: 10.1128/jb.137.3.1271-1281.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 8. Microbiol Rev. 1990 Jun;54(2):130–197. doi: 10.1128/mr.54.2.130-197.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bender J., Kleckner N. IS10 transposase mutations that specifically alter target site recognition. EMBO J. 1992 Feb;11(2):741–750. doi: 10.1002/j.1460-2075.1992.tb05107.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Benson N. R., Goldman B. S. Rapid mapping in Salmonella typhimurium with Mud-P22 prophages. J Bacteriol. 1992 Mar;174(5):1673–1681. doi: 10.1128/jb.174.5.1673-1681.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bi E., Lutkenhaus J. Interaction between the min locus and ftsZ. J Bacteriol. 1990 Oct;172(10):5610–5616. doi: 10.1128/jb.172.10.5610-5616.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bochner B. R., Ames B. N. ZTP (5-amino 4-imidazole carboxamide riboside 5'-triphosphate): a proposed alarmone for 10-formyl-tetrahydrofolate deficiency. Cell. 1982 Jul;29(3):929–937. doi: 10.1016/0092-8674(82)90455-x. [DOI] [PubMed] [Google Scholar]
  10. Bochner B. R., Huang H. C., Schieven G. L., Ames B. N. Positive selection for loss of tetracycline resistance. J Bacteriol. 1980 Aug;143(2):926–933. doi: 10.1128/jb.143.2.926-933.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brown E. A., D'Ari R., Newman E. B. A relationship between L-serine degradation and methionine biosynthesis in Escherichia coli K12. J Gen Microbiol. 1990 Jun;136(6):1017–1023. doi: 10.1099/00221287-136-6-1017. [DOI] [PubMed] [Google Scholar]
  12. Casadesus J., Roth J. R. Absence of insertions among spontaneous mutants of Salmonella typhimurium. Mol Gen Genet. 1989 Apr;216(2-3):210–216. doi: 10.1007/BF00334358. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. 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]
  15. Ciampi M. S., Schmid M. B., Roth J. R. Transposon Tn10 provides a promoter for transcription of adjacent sequences. Proc Natl Acad Sci U S A. 1982 Aug;79(16):5016–5020. doi: 10.1073/pnas.79.16.5016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Csonka L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. doi: 10.1128/mr.53.1.121-147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Csonka L. N. Proline over-production results in enhanced osmotolerance in Salmonella typhimurium. Mol Gen Genet. 1981;182(1):82–86. doi: 10.1007/BF00422771. [DOI] [PubMed] [Google Scholar]
  18. Donachie W. D., Begg K. J., Vicente M. Cell length, cell growth and cell division. Nature. 1976 Nov 25;264(5584):328–333. doi: 10.1038/264328a0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. Fink G. R., Klopotowski T., Ames B. N. Histidine regulatory mutants in Salmonella typhimurium. IV. A positive selection for polar histidine-requiring mutants from histidine operator constitutive mutants. J Mol Biol. 1967 Nov 28;30(1):81–95. doi: 10.1016/0022-2836(67)90245-8. [DOI] [PubMed] [Google Scholar]
  21. Flores A., Fox M., Casadesús J. The pleiotropic effects of his overexpression in Salmonella typhimurium do not involve AICAR-induced mutagenesis. Mol Gen Genet. 1993 Sep;240(3):360–364. doi: 10.1007/BF00280387. [DOI] [PubMed] [Google Scholar]
  22. Fox M., Frandsen N., D'Ari R. AICAR is not an endogenous mutagen in Escherichia coli. Mol Gen Genet. 1993 Sep;240(3):355–359. doi: 10.1007/BF00280386. [DOI] [PubMed] [Google Scholar]
  23. Frandsen N., D'Ari R. Excess histidine enzymes cause AICAR-independent filamentation in Escherichia coli. Mol Gen Genet. 1993 Sep;240(3):348–354. doi: 10.1007/BF00280385. [DOI] [PubMed] [Google Scholar]
  24. Gibert I., Casadesús J. sulA-independent division inhibition in his-constitutive strains of Salmonella typhimurium. FEMS Microbiol Lett. 1990 Jun 1;57(3):205–210. doi: 10.1016/0378-1097(90)90066-y. [DOI] [PubMed] [Google Scholar]
  25. Gutnick D., Calvo J. M., Klopotowski T., Ames B. N. Compounds which serve as the sole source of carbon or nitrogen for Salmonella typhimurium LT-2. J Bacteriol. 1969 Oct;100(1):215–219. doi: 10.1128/jb.100.1.215-219.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hartman P. E., Roth J. R. Mechanisms of suppression. Adv Genet. 1973;17:1–105. doi: 10.1016/s0065-2660(08)60170-4. [DOI] [PubMed] [Google Scholar]
  27. Hill C. W., Schiffer D., Berg P. Transduction of merodiploidy: induced duplication of recipient genes. J Bacteriol. 1969 Jul;99(1):274–278. doi: 10.1128/jb.99.1.274-278.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Hughes K. T., Roth J. R. Directed formation of deletions and duplications using Mud(Ap, lac). Genetics. 1985 Feb;109(2):263–282. doi: 10.1093/genetics/109.2.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hughes K. T., Roth J. R. Transitory cis complementation: a method for providing transposition functions to defective transposons. Genetics. 1988 May;119(1):9–12. doi: 10.1093/genetics/119.1.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Kleckner N., Roth J., Botstein D. Genetic engineering in vivo using translocatable drug-resistance elements. New methods in bacterial genetics. J Mol Biol. 1977 Oct 15;116(1):125–159. doi: 10.1016/0022-2836(77)90123-1. [DOI] [PubMed] [Google Scholar]
  33. Kohno T., Roth J. Electrolyte effects on the activity of mutant enzymes in vivo and in vitro. Biochemistry. 1979 Apr 3;18(7):1386–1392. doi: 10.1021/bi00574a041. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Morisato D., Way J. C., Kim H. J., Kleckner N. Tn10 transposase acts preferentially on nearby transposon ends in vivo. Cell. 1983 Mar;32(3):799–807. doi: 10.1016/0092-8674(83)90066-1. [DOI] [PubMed] [Google Scholar]
  36. Murray M. L., Hartman P. E. Overproduction of hisH and hisF gene products leads to inhibition of cell cell division in Salmonella. Can J Microbiol. 1972 May;18(5):671–681. doi: 10.1139/m72-105. [DOI] [PubMed] [Google Scholar]
  37. Newell P. C., Tucker R. G. Biosynthesis of the pyrimidine moiety of thiamine. A new route of pyrimidine biosynthesis involving purine intermediates. Biochem J. 1968 Jan;106(1):279–287. doi: 10.1042/bj1060279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rupp W. D., Wilde C. E., 3rd, Reno D. L., Howard-Flanders P. Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli. J Mol Biol. 1971 Oct 14;61(1):25–44. doi: 10.1016/0022-2836(71)90204-x. [DOI] [PubMed] [Google Scholar]
  39. Sabina R. L., Holmes E. W., Becker M. A. The enzymatic synthesis of 5-amino-4-imidazolecarboxamide riboside triphosphate (ZTP). Science. 1984 Mar 16;223(4641):1193–1195. doi: 10.1126/science.6199843. [DOI] [PubMed] [Google Scholar]
  40. Sanderson K. E., Roth J. R. Linkage map of Salmonella typhimurium, edition VII. Microbiol Rev. 1988 Dec;52(4):485–532. doi: 10.1128/mr.52.4.485-532.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schmid M. B., Roth J. R. Internal promoters of the his operon in Salmonella typhimurium. J Bacteriol. 1983 Feb;153(2):1114–1119. doi: 10.1128/jb.153.2.1114-1119.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Schmieger H. Phage P22-mutants with increased or decreased transduction abilities. Mol Gen Genet. 1972;119(1):75–88. doi: 10.1007/BF00270447. [DOI] [PubMed] [Google Scholar]
  43. Simons R. W., Hoopes B. C., McClure W. R., Kleckner N. Three promoters near the termini of IS10: pIN, pOUT, and pIII. Cell. 1983 Sep;34(2):673–682. doi: 10.1016/0092-8674(83)90400-2. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. 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]
  46. de Boer P. A., Crossley R. E., Rothfield L. I. Isolation and properties of minB, a complex genetic locus involved in correct placement of the division site in Escherichia coli. J Bacteriol. 1988 May;170(5):2106–2112. doi: 10.1128/jb.170.5.2106-2112.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES