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PMID: 2144275 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Sequence analysis and mapping of the Salmonella typhimurium LT2 umuDC operon.

Journal of bacteriology ·Vol. 172 ·No. 9 ·1990-09-00 ·Pages 4964-78

Smith CM, Koch WH, Franklin SB, Foster PL, Cebula TA, Eisenstadt E

Abstract

In Escherichia coli, efficient mutagenesis by UV requires the umuDC operon. A deficiency in umuDC activity is believed to be responsible for the relatively weak UV mutability of Salmonella typhimurium LT2 compared with that of E. coli. To begin evaluating this hypothesis and the evolutionary relationships among umuDC-related sequences, we cloned and sequenced the S. typhimurium umuDC operon. S. typhimurium umuDC restored mutability to umuD and umuC mutants of E. coli. DNA sequence analysis of 2,497 base pairs (bp) identified two nonoverlapping open reading frames spanning 1,691 bp that were were 67 and 72% identical at the nucleotide sequence level to the umuD and umuC sequences, respectively, from E. coli. The sequences encoded proteins whose deduced primary structures were 73 and 84% identical to the E. coli umuD and umuC gene products, respectively. The two bacterial umuDC sequences were more similar to each other than to mucAB, a plasmid-borne umuDC homolog. The umuD product retained the Cys-24--Gly-25, Ser-60, and Lys-97 amino acid residues believed to be critical for RecA-mediated proteolytic activation of UmuD. The presence of a LexA box 17 bp upstream from the UmuD initiation codon suggests that this operon is a member of an SOS regulon. Mu d-P22 inserts were used to locate the S. typhimurium umuDC operon to a region between 35.9 and 40 min on the S. typhimurium chromosome. In E. coli, umuDC is located at 26 min. The umuDC locus in S. typhimurium thus appears to be near one end of a chromosomal inversion that distinguishes gene order in the 25- to 35-min regions of the E. coli and S. typhimurium chromosomes. It is likely, therefore, that the umuDC operon was present in a common ancestor before S. typhimurium and E. coli diverged approximately 150 million years ago. These results provide new information for investigating the structure, function, and evolutionary origins of umuDC and for exploring the genetic basis for the mutability differences between S. typhimurium and E. coli.

MeSH Terms
Amino Acid Sequence Bacteriophage lambda/genetics Base Sequence DNA, Bacterial/genetics,isolation & purification DNA, Viral/genetics,isolation & purification Escherichia coli/genetics,radiation effects Gene Library Molecular Sequence Data Nucleic Acid Hybridization Oligonucleotide Probes Operon Plasmids Restriction Mapping Salmonella typhimurium/genetics,radiation effects Sequence Homology, Nucleic Acid Ultraviolet Rays
Chemicals
DNA, Bacterial DNA, Viral Oligonucleotide Probes
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Smith C M
Interdisciplinary Programs in Health, Harvard School of Public Health, Boston, Massachusetts.
Koch W H
Franklin S B
Foster P L
Cebula T A
Eisenstadt E
References (61)
61 references, click to expand
  1. Plasmids of Escherichia coli as cloning vectors.
    Methods Enzymol. 1979;68:245-67 PMID: 232214
  2. groE mutants of Escherichia coli are defective in umuDC-dependent UV mutagenesis.
    J Bacteriol. 1989 Nov;171(11):6117-25 PMID: 2572581
  3. Distribution among incompatibility groups of plasmids that confer UV mutability and UV resistance.
    Mutat Res. 1980 Aug;72(1):155-9 PMID: 6777687
  4. Role of the supX gene in ultraviolet light-induced mutagenesis in Salmonella typhimurium.
    J Bacteriol. 1981 Apr;146(1):170-8 PMID: 7012113
  5. UV-mutable hybrids of Salmonella incorporating Escherichia coli region adjacent to tryptophan operon.
    Mol Gen Genet. 1982;185(2):315-8 PMID: 7045586
  6. Regulation and functions of Escherichia coli genes induced by DNA damage.
    Basic Life Sci. 1982;20:43-63 PMID: 6287997
  7. Rapid similarity searches of nucleic acid and protein data banks.
    Proc Natl Acad Sci U S A. 1983 Feb;80(3):726-30 PMID: 6572363
  8. The SOS regulatory system: control of its state by the level of RecA protease.
    J Mol Biol. 1983 Jul 15;167(4):791-808 PMID: 6410076
  9. Inducible repair of oxidative DNA damage in Escherichia coli.
    Nature. 1983 Aug 4-10;304(5925):466-8 PMID: 6348554
  10. Cloning and characterization of the umu operon responsible for inducible mutagenesis in Escherichia coli.
    Gene. 1983 Aug;23(2):167-74 PMID: 6311684
  11. Expression of eight unrelated Muc+ plasmids in eleven DNA repair-deficient E. coli strains.
    Mutat Res. 1983 Oct;112(5):261-73 PMID: 6314133
  12. Autodigestion of lexA and phage lambda repressors.
    Proc Natl Acad Sci U S A. 1984 Mar;81(5):1375-9 PMID: 6231641
  13. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli.
    Microbiol Rev. 1984 Mar;48(1):60-93 PMID: 6371470
  14. Catabolic alanine racemase from Salmonella typhimurium: DNA sequence, enzyme purification, and characterization.
    Biochemistry. 1984 Oct 23;23(22):5182-7 PMID: 6391537
  15. Cold sensitivity induced by overproduction of UmuDC in Escherichia coli.
    J Bacteriol. 1985 Apr;162(1):155-61 PMID: 2984171
  16. Chromosomal location and evolutionary rate variation in enterobacterial genes.
    Science. 1989 Nov 10;246(4931):808-10 PMID: 2683084
  17. Autodigestion and RecA-dependent cleavage of Ind- mutant LexA proteins.
    J Mol Biol. 1989 Dec 5;210(3):439-52 PMID: 2693734
  18. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication.
    J Mol Biol. 1990 Mar 5;212(1):79-96 PMID: 2108251
  19. Alignment of Escherichia coli K12 DNA sequences to a genomic restriction map.
    Nucleic Acids Res. 1990 Jan 25;18(2):313-21 PMID: 2183179
  20. Linkage map of Escherichia coli K-12, edition 8.
    Microbiol Rev. 1990 Jun;54(2):130-97 PMID: 2194094
  21. Structural characterization of the Salmonella typhimurium LT2 umu operon.
    J Bacteriol. 1990 Sep;172(9):4979-87 PMID: 2203737
  22. Differences in mutagenic and recombinational DNA repair in enterobacteria.
    Proc Natl Acad Sci U S A. 1985 Jun;82(12):4172-6 PMID: 3858873
  23. Positive control of a regulon for defenses against oxidative stress and some heat-shock proteins in Salmonella typhimurium.
    Cell. 1985 Jul;41(3):753-62 PMID: 2988786
  24. A general method applicable to the search for similarities in the amino acid sequence of two proteins.
    J Mol Biol. 1970 Mar;48(3):443-53 PMID: 5420325
  25. Transformation of Salmonella typhimurium by plasmid deoxyribonucleic acid.
    J Bacteriol. 1974 Sep;119(3):1072-4 PMID: 4605400
  26. Gene rearrangements in the evolution of the tryptophan synthetic pathway.
    Bacteriol Rev. 1975 Jun;39(2):87-120 PMID: 806280
  27. Mutagenic DNA repair in Escherichia coli. III. Requirement for a function of DNA polymerase III in ultraviolet-light mutagenesis.
    Mol Gen Genet. 1976 Feb 27;144(1):53-8 PMID: 772414
  28. Ultraviolet light protection, enhancement of ultraviolet light mutagenesis, and mutator effect of plasmid R46 in Salmonella typhimurium.
    J Bacteriol. 1976 Oct;128(1):271-82 PMID: 789333
  29. Isolation and characterization of mutants of Escherichia coli deficient in induction of mutations by ultraviolet light.
    Mol Gen Genet. 1977 Nov 14;156(2):121-31 PMID: 340898
  30. Inducible reactivation and mutagenesis of UV-irradiated bacteriophage P22 in Salmonella typhimurium LT2 containing the plasmid pKM101.
    J Bacteriol. 1978 Aug;135(2):415-21 PMID: 355224
  31. Nucleotide sequence binding specificity of the LexA repressor of Escherichia coli K-12.
    J Bacteriol. 1985 Jul;163(1):376-84 PMID: 3891738
  32. umuDC and mucAB operons whose products are required for UV light- and chemical-induced mutagenesis: UmuD, MucA, and LexA proteins share homology.
    Proc Natl Acad Sci U S A. 1985 Jul;82(13):4331-5 PMID: 2989816
  33. Structural analysis of the umu operon required for inducible mutagenesis in Escherichia coli.
    Proc Natl Acad Sci U S A. 1985 Jul;82(13):4336-40 PMID: 2989817
  34. Involvement of helicase II (uvrD gene product) and DNA polymerase I in excision mediated by the uvrABC protein complex.
    Proc Natl Acad Sci U S A. 1985 Aug;82(15):4925-9 PMID: 3161077
  35. Genes from plasmid pKM101 in Haemophilus influenzae: separation of functions of mucA and mucB.
    Proc Natl Acad Sci U S A. 1985 Nov;82(22):7753-6 PMID: 3877933
  36. Lambda repressor inactivation: properties of purified ind- proteins in the autodigestion and RecA-mediated cleavage reactions.
    J Mol Biol. 1986 Nov 5;192(1):39-47 PMID: 3820305
  37. Gene location affects expression level in Salmonella typhimurium.
    J Bacteriol. 1987 Jun;169(6):2872-5 PMID: 3294809
  38. An inducible pathway is required for mutagenesis in Salmonella typhimurium LT2.
    J Bacteriol. 1987 Jun;169(6):2885-8 PMID: 3294811
  39. Lysine-156 and serine-119 are required for LexA repressor cleavage: a possible mechanism.
    Proc Natl Acad Sci U S A. 1987 Jun;84(12):3987-91 PMID: 3108885
  40. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library.
    Cell. 1987 Jul 31;50(3):495-508 PMID: 3038334
  41. Inactivation of isocitrate dehydrogenase by phosphorylation is mediated by the negative charge of the phosphate.
    J Biol Chem. 1987 Aug 5;262(22):10422-5 PMID: 3112144
  42. Plasmid genes affecting DNA repair and mutation.
    J Cell Sci Suppl. 1987;6:303-21 PMID: 3308922
  43. Oligonucleotide probes for the screening of recombinant DNA libraries.
    Methods Enzymol. 1987;152:432-42 PMID: 3309569
  44. Derepression of specific genes promotes DNA repair and mutagenesis in Escherichia coli.
    J Bacteriol. 1988 Jan;170(1):1-4 PMID: 3275605
  45. Isolation of Salmonella typhimurium cys genes by transduction with a library of recombinant plasmids packaged in bacteriophage P22HT capsids.
    J Bacteriol. 1988 Jan;170(1):42-7 PMID: 3275623
  46. RecA protein-dependent cleavage of UmuD protein and SOS mutagenesis.
    Proc Natl Acad Sci U S A. 1988 Mar;85(6):1806-10 PMID: 3126496
  47. UmuD mutagenesis protein of Escherichia coli: overproduction, purification, and cleavage by RecA.
    Proc Natl Acad Sci U S A. 1988 Mar;85(6):1811-5 PMID: 3279417
  48. RecA-mediated cleavage activates UmuD for mutagenesis: mechanistic relationship between transcriptional derepression and posttranslational activation.
    Proc Natl Acad Sci U S A. 1988 Mar;85(6):1816-20 PMID: 3279418
  49. Polymorphisms in the umuDC region of Escherichia species.
    J Bacteriol. 1988 Apr;170(4):1610-6 PMID: 2895099
  50. UV-light-induced mutability in Salmonella strains containing the umuDC or the mucAB operon: evidence for a umuC function.
    Mutat Res. 1988 Mar;198(1):9-13 PMID: 2832752
  51. Packaging specific segments of the Salmonella chromosome with locked-in Mud-P22 prophages.
    Genetics. 1988 Apr;118(4):581-92 PMID: 2835289
  52. DNA sequencing with Thermus aquaticus DNA polymerase and direct sequencing of polymerase chain reaction-amplified DNA.
    Proc Natl Acad Sci U S A. 1988 Dec;85(24):9436-40 PMID: 3200828
  53. Lack of umuDC gene functions in Vibrio cholerae cells.
    Mutat Res. 1989 Jan;210(1):149-56 PMID: 2642599
  54. Interactions between epsilon, the proofreading subunit of DNA polymerase III, and proteins involved in the SOS response of Escherichia coli.
    Mol Gen Genet. 1988 Nov;214(3):467-73 PMID: 2851096
  55. Linkage map of Salmonella typhimurium, edition VII.
    Microbiol Rev. 1988 Dec;52(4):485-532 PMID: 3070321
  56. Identification of a umuDC locus in Salmonella typhimurium LT2.
    J Bacteriol. 1989 Jul;171(7):3860-5 PMID: 2661537
  57. Use of the isocitrate dehydrogenase structural gene for attachment of e14 in Escherichia coli K-12.
    J Bacteriol. 1989 Jul;171(7):4083-4 PMID: 2661545
  58. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):5054-8 PMID: 2544889
  59. UmuC mutagenesis protein of Escherichia coli: purification and interaction with UmuD and UmuD'.
    Proc Natl Acad Sci U S A. 1989 Oct;86(19):7301-5 PMID: 2552436
  60. Cloning of Salmonella typhimurium DNA encoding mutagenic DNA repair.
    J Bacteriol. 1989 Nov;171(11):5776-82 PMID: 2681141
  61. Cleavage of the Escherichia coli lexA protein by the recA protease.
    Proc Natl Acad Sci U S A. 1980 Jun;77(6):3225-9 PMID: 6447873
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1990-09-00
Pages
4964-78
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC213152
Subset
IM
Grants
NCI NIH HHS · CA37880 · United States
Databases
GENBANK
M35010, M57431
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