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PMID: 7751283 Published · ppublish English Comparative Study Journal Article

Characterization of the umu-complementing operon from R391.

Journal of bacteriology ·Vol. 177 ·No. 10 ·1995-05-00 ·Pages 2737-43

Kulaeva OI, Wootton JC, Levine AS, Woodgate R

Abstract

In addition to conferring resistances to antibiotics and heavy metals, certain R factors carry genes involved in mutagenic DNA repair. These plasmid-encoded genes are structurally and functionally related to the chromosomally encoded umuDC genes of Escherichia coli and Salmonella typhimurium. Three such plasmid operons, mucAB, impCAB, and samAB, have been characterized at the molecular level. Recently, we have identified three additional umu-complementing operons from IncJ plasmid R391 and IncL/M plasmids R446b and R471a. We report here the molecular characterization of the R391 umu-complementing operon. The nucleotide sequence of the minimal R plasmid umu-complementing (rum) region revealed an operon of two genes, rumA(R391) and rumB(R391), with an upstream regulatory signal strongly resembling LexA-binding sites. Phylogenetic analysis revealed that the RumAB(R391) proteins are approximately equally diverged in sequence from the chromosomal UmuDC proteins and the other plasmid-encoded Umu-like proteins and represent a new subfamily. Genetic characterization of the rumAB(R391) operon revealed that in recA+ and recA1730 backgrounds, the rumAB(R391) operon was phenotypically indistinguishable from mucAB. In contrast, however, the rumAB(R391) operon gave levels of mutagenesis that were intermediate between those given by mucAB and umuDC in a recA430 strain. The latter phenotype was shown to correlate with the reduced posttranslational processing of the RumA(R391) protein to its mutagenically active form, RumA'(R391). Thus, the rumAB(R391) operon appears to possess characteristics that are reminiscent of both chromosome and plasmid-encoded umu-like operons.

Related Genes
MeSH Terms
Amino Acid Sequence Bacterial Proteins/genetics Base Sequence DNA Repair/genetics DNA-Directed DNA Polymerase Escherichia coli/genetics,radiation effects Escherichia coli Proteins Genes, Bacterial/genetics Genetic Complementation Test Molecular Sequence Data Mutagenesis/genetics Operon/genetics Phylogeny R Factors/genetics Regulatory Sequences, Nucleic Acid/genetics Sequence Analysis, DNA Sequence Homology, Amino Acid Ultraviolet Rays
Chemicals
Bacterial Proteins Escherichia coli Proteins MucA protein, Bacteria MucB protein, Bacteria RumA protein, Bacteria RumB protein, E coli UmuC protein, E coli DNA-Directed DNA Polymerase UmuD protein, E coli
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Kulaeva O I
Section on DNA Replication, Repair and Mutagenesis, National Institute of Child Health and Human Development, NIH, Bethesda, MD 20892-2725, USA.
Wootton J C
Levine A S
Woodgate R
References (53)
53 references, click to expand
  1. Spontaneous, ultraviolet and ionizing radiation mutagenesis in two auxotrophic strains of Salmonella typhimurium carrying an R plasmid.
    Mutat Res. 1977 Oct;45(1):1-6 PMID: 335234
  2. Deoxyribonucleic acid base composition of Proteus and Providence organisms.
    J Bacteriol. 1962 Jun;83:1318-21 PMID: 13891463
  3. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  4. Distribution among incompatibility groups of plasmids that confer UV mutability and UV resistance.
    Mutat Res. 1980 Aug;72(1):155-9 PMID: 6777687
  5. Role of the supX gene in ultraviolet light-induced mutagenesis in Salmonella typhimurium.
    J Bacteriol. 1981 Apr;146(1):170-8 PMID: 7012113
  6. Plasmid pKM101-dependent repair and mutagenesis in Escherichia coli cells with mutations lexB30 tif and zab-53 in the recA gene.
    Mutat Res. 1981 May;81(3):265-75 PMID: 7029254
  7. UV-mutable hybrids of Salmonella incorporating Escherichia coli region adjacent to tryptophan operon.
    Mol Gen Genet. 1982;185(2):315-8 PMID: 7045586
  8. Influence of RecA protein on induced mutagenesis.
    Biochimie. 1982 Aug-Sep;64(8-9):633-6 PMID: 6814511
  9. Identification of plasmid (pKM101)-coded proteins involved in mutagenesis and UV resistance.
    Nature. 1982 Nov 18;300(5889):278-81 PMID: 6755263
  10. Expression of eight unrelated Muc+ plasmids in eleven DNA repair-deficient E. coli strains.
    Mutat Res. 1983 Oct;112(5):261-73 PMID: 6314133
  11. Autodigestion of lexA and phage lambda repressors.
    Proc Natl Acad Sci U S A. 1984 Mar;81(5):1375-9 PMID: 6231641
  12. Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli.
    Microbiol Rev. 1984 Mar;48(1):60-93 PMID: 6371470
  13. The effect of plasmid R391 and other IncJ plasmids on the survival of Escherichia coli after UV irradiation.
    J Gen Microbiol. 1984 Jul;130(7):1839-44 PMID: 6381648
  14. The two-step model of bacterial UV mutagenesis.
    Mutat Res. 1985 Jun-Jul;150(1-2):133-9 PMID: 4000157
  15. Complementation of a pKM101 derivative that decreases resistance to UV killing but increases susceptibility to mutagenesis.
    Mutat Res. 1985 Jun-Jul;150(1-2):147-58 PMID: 2987687
  16. Dual role for Escherichia coli RecA protein in SOS mutagenesis.
    Proc Natl Acad Sci U S A. 1985 May;82(10):3325-9 PMID: 3159017
  17. Differences in mutagenic and recombinational DNA repair in enterobacteria.
    Proc Natl Acad Sci U S A. 1985 Jun;82(12):4172-6 PMID: 3858873
  18. Mutagenic repair in Escherichia coli: products of the recA gene and of the umuD and umuC genes act at different steps in UV-induced mutagenesis.
    Proc Natl Acad Sci U S A. 1985 Jun;82(12):4193-7 PMID: 3889923
  19. 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
  20. 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
  21. Enhancement of UV survival, UV- and MMS-mutability, precise excision of Tn10 and complementation of umuC by plasmids of different incompatibility groups.
    Mutat Res. 1986 Jul;166(1):29-37 PMID: 3014325
  22. Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure.
    J Bacteriol. 1987 Feb;169(2):751-7 PMID: 3027045
  23. Different efficiency of UmuDC and MucAB proteins in UV light induced mutagenesis in Escherichia coli.
    Mol Gen Genet. 1986 Nov;205(2):234-9 PMID: 3027502
  24. An inducible pathway is required for mutagenesis in Salmonella typhimurium LT2.
    J Bacteriol. 1987 Jun;169(6):2885-8 PMID: 3294811
  25. 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
  26. 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
  27. 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
  28. 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
  29. Phylogenies from molecular sequences: inference and reliability.
    Annu Rev Genet. 1988;22:521-65 PMID: 3071258
  30. Identification of a umuDC locus in Salmonella typhimurium LT2.
    J Bacteriol. 1989 Jul;171(7):3860-5 PMID: 2661537
  31. Cloning of Salmonella typhimurium DNA encoding mutagenic DNA repair.
    J Bacteriol. 1989 Nov;171(11):5776-82 PMID: 2681141
  32. Use of T7 RNA polymerase to direct expression of cloned genes.
    Methods Enzymol. 1990;185:60-89 PMID: 2199796
  33. Sequence analysis and mapping of the Salmonella typhimurium LT2 umuDC operon.
    J Bacteriol. 1990 Sep;172(9):4964-78 PMID: 2144275
  34. Structural characterization of the Salmonella typhimurium LT2 umu operon.
    J Bacteriol. 1990 Sep;172(9):4979-87 PMID: 2203737
  35. DNA sequence analysis of the imp UV protection and mutation operon of the plasmid TP110: identification of a third gene.
    Nucleic Acids Res. 1990 Sep 11;18(17):5045-50 PMID: 2129552
  36. Salmonella typhimurium has two homologous but different umuDC operons: cloning of a new umuDC-like operon (samAB) present in a 60-megadalton cryptic plasmid of S. typhimurium.
    J Bacteriol. 1991 Feb;173(3):1051-63 PMID: 1991707
  37. Distribution of sequences homologous to the impCAB operon of TP110 among bacterial plasmids of different incompatibility groups.
    Mol Gen Genet. 1991 Sep;229(1):27-30 PMID: 1680217
  38. R factors from Proteus rettgeri.
    J Gen Microbiol. 1972 Oct;72(3):543-52 PMID: 4564689
  39. Survival, mutation and capacity to repair single-strand DNA breaks after gamma irradiation in different Exr - strains of Escherichia coli.
    Mol Gen Genet. 1972;119(2):93-102 PMID: 4565757
  40. A RecA protein mutant deficient in its interaction with the UmuDC complex.
    Biochimie. 1991 Apr;73(4):479-84 PMID: 1911948
  41. Functional complementation between chromosomal and plasmid mutagenic DNA repair genes in bacteria.
    Mol Gen Genet. 1991 Oct;229(3):428-36 PMID: 1658597
  42. Construction of a umuDC operon substitution mutation in Escherichia coli.
    Mutat Res. 1992 Mar;281(3):221-5 PMID: 1371846
  43. UV mutagenesis in Salmonella typhimurium is umuDC dependent despite the presence of samAB.
    J Bacteriol. 1992 May;174(9):2809-15 PMID: 1569012
  44. A partially deficient mutant, recA1730, that fails to form normal nucleoprotein filaments.
    Mol Gen Genet. 1992 Apr;232(3):489-97 PMID: 1534140
  45. The enhanced mutagenic potential of the MucAB proteins correlates with the highly efficient processing of the MucA protein.
    J Bacteriol. 1992 Nov;174(21):6844-51 PMID: 1400235
  46. Roles of Salmonella typhimurium umuDC and samAB in UV mutagenesis and UV sensitivity.
    J Bacteriol. 1992 Nov;174(21):6948-55 PMID: 1400244
  47. Mutagenesis induced by bacterial UmuDC proteins and their plasmid homologues.
    Mol Microbiol. 1992 Aug;6(16):2213-8 PMID: 1406263
  48. Activity of the purified mutagenesis proteins UmuC, UmuD', and RecA in replicative bypass of an abasic DNA lesion by DNA polymerase III.
    Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10777-81 PMID: 1438275
  49. A rapid method for cloning mutagenic DNA repair genes: isolation of umu-complementing genes from multidrug resistance plasmids R391, R446b, and R471a.
    J Bacteriol. 1993 Sep;175(17):5411-9 PMID: 8366028
  50. Targeting of the UmuD, UmuD', and MucA' mutagenesis proteins to DNA by RecA protein.
    Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8169-73 PMID: 8367479
  51. SOS mutagenesis.
    Curr Opin Genet Dev. 1993 Oct;3(5):719-25 PMID: 8274853
  52. Isolation and characterization of novel plasmid-encoded umuC mutants.
    J Bacteriol. 1994 Aug;176(16):5011-21 PMID: 8051014
  53. 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
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1995-05-00
Pages
2737-43
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC176944
Subset
IM
Databases
GENBANK
U13633
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