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PMID: 16030214 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

A DNA polymerase V homologue encoded by TOL plasmid pWW0 confers evolutionary fitness on Pseudomonas putida under conditions of environmental stress.

Journal of bacteriology ·Vol. 187 ·No. 15 ·2005-08-00 ·Pages 5203-13

Tark M, Tover A, Tarassova K, Tegova R, Kivi G, Hõrak R, Kivisaar M

Abstract

Plasmids in conjunction with other mobile elements such as transposons are major players in the genetic adaptation of bacteria in response to changes in environment. Here we show that a large catabolic TOL plasmid, pWW0, from Pseudomonas putida carries genes (rulAB genes) encoding an error-prone DNA polymerase Pol V homologue which increase the survival of bacteria under conditions of accumulation of DNA damage. A study of population dynamics in stationary phase revealed that the presence of pWW0-derived rulAB genes in the bacterial genome allows the expression of a strong growth advantage in stationary phase (GASP) phenotype of P. putida. When rulAB-carrying cells from an 8-day-old culture were mixed with Pol V-negative cells from a 1-day-old culture, cells derived from the aged culture out-competed cells from the nonaged culture and overtook the whole culture. At the same time, bacteria from an aged culture lacking the rulAB genes were only partially able to out-compete cells from a fresh overnight culture of the parental P. putida strain. Thus, in addition to conferring resistance to DNA damage, the plasmid-encoded Pol V genes significantly increase the evolutionary fitness of bacteria during prolonged nutritional starvation of a P. putida population. The results of our study indicate that RecA is involved in the control of expression of the pWW0-encoded Pol V.

MeSH Terms
Adaptation, Physiological/genetics Base Sequence Biological Evolution DNA-Directed DNA Polymerase/genetics Escherichia coli Proteins Molecular Sequence Data Plasmids/genetics Pseudomonas putida/genetics,growth & development Sequence Alignment Time Factors
Chemicals
Escherichia coli Proteins DNA polymerase V, E coli DNA-Directed DNA Polymerase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Tark Mariliis
Department of Genetics, Institute of Molecular and Cell Biology, Tartu University and Estonian Biocentre, 23 Riia Street, 51010 Tartu, Estonia.
Tover Andres
Tarassova Kairi
Tegova Radi
Kivi Gaily
Hõrak Rita
Kivisaar Maia
References (73)
73 references, click to expand
  1. Roles of the mutagenesis proteins SamA'B and MucA'B in chemically induced frameshift mutagenesis in Salmonella typhimurium hisD3052.
    Mutat Res. 1998 Feb 26;398(1-2):33-42 PMID: 9626963
  2. Enzymes of evolutionary change.
    Nature. 1999 Oct 28;401(6756):866-7, 869 PMID: 10553899
  3. Involvement of error-prone DNA polymerase IV in stationary-phase mutagenesis in Pseudomonas putida.
    J Bacteriol. 2004 May;186(9):2735-44 PMID: 15090515
  4. Managing DNA polymerases: coordinating DNA replication, DNA repair, and DNA recombination.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8342-9 PMID: 11459973
  5. The distribution of the numbers of mutants in bacterial populations.
    J Genet. 1949 Dec;49(3):264-85 PMID: 24536673
  6. Plasmid-encoded MucB protein is a DNA polymerase (pol RI) specialized for lesion bypass in the presence of MucA', RecA, and SSB.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11227-31 PMID: 11016960
  7. Identification and characterization of Tn4653, a transposon covering the toluene transposon Tn4651 on TOL plasmid pWW0.
    Mol Gen Genet. 1988 Jul;213(1):72-7 PMID: 2851712
  8. Evolution of microbial diversity during prolonged starvation.
    Proc Natl Acad Sci U S A. 1999 Mar 30;96(7):4023-7 PMID: 10097156
  9. 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
  10. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli.
    Genetics. 2001 May;158(1):41-64 PMID: 11333217
  11. Induction of mutation in Escherichia coli by freeze-drying.
    Appl Environ Microbiol. 1979 Mar;37(3):369-72 PMID: 378126
  12. An aromatic effector specificity mutant of the transcriptional regulator DmpR overcomes the growth constraints of Pseudomonas sp. strain CF600 on para-substituted methylphenols.
    J Bacteriol. 1994 Dec;176(24):7550-7 PMID: 8002579
  13. Two modes of loss of the Tol function from Pseudomonas putida mt-2.
    Mol Gen Genet. 1977 Jul 20;154(2):203-4 PMID: 895716
  14. Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators.
    Annu Rev Microbiol. 1997;51:341-73 PMID: 9343354
  15. Increased mutagenesis mediated by cloned plasmid CAM-OCT genes: potential for expanding substrate ranges of Pseudomonas spp.
    Appl Environ Microbiol. 1996 Sep;62(9):3538-40 PMID: 8795249
  16. One-step cloning system for isolation of bacterial lexA-like genes.
    J Bacteriol. 1991 Nov;173(22):7345-50 PMID: 1938926
  17. Characterization of a new LexA binding motif in the marine magnetotactic bacterium strain MC-1.
    J Bacteriol. 2003 Aug;185(15):4471-82 PMID: 12867456
  18. The growth of micro-organisms in relation to their energy supply.
    J Gen Microbiol. 1960 Dec;23:457-69 PMID: 13687855
  19. Intermolecular cleavage by UmuD-like mutagenesis proteins.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1478-83 PMID: 9465040
  20. 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
  21. Preparation of electrocompetent E. coli using salt-free growth medium.
    Biotechniques. 1996 Jan;20(1):42-4 PMID: 8770403
  22. Resistance to ultraviolet light in Pseudomonas syringae: sequence and functional analysis of the plasmid-encoded rulAB genes.
    Gene. 1996 Oct 24;177(1-2):77-81 PMID: 8921848
  23. Role of DNA repair genes and an R plasmid in conferring cryoresistance on Pseudomonas aeruginosa.
    J Gen Microbiol. 1982 Jan;128(1):215-8 PMID: 6806439
  24. Inducible UV repair potential of Pseudomonas aeruginosa PAO.
    J Gen Microbiol. 1990 Jul;136(7):1241-9 PMID: 2121899
  25. Regulation of the transposase of Tn4652 by the transposon-encoded protein TnpC.
    J Bacteriol. 1999 Oct;181(20):6312-8 PMID: 10515920
  26. Expression of the transposase gene tnpA of Tn4652 is positively affected by integration host factor.
    J Bacteriol. 1998 Jun;180(11):2822-9 PMID: 9603867
  27. Metabolism of benzoate and the methylbenzoates by Pseudomonas putida (arvilla) mt-2: evidence for the existence of a TOL plasmid.
    J Bacteriol. 1974 Oct;120(1):416-23 PMID: 4418209
  28. Functional analysis of the Pseudomonas syringae rulAB determinant in tolerance to ultraviolet B (290-320 nm) radiation and distribution of rulAB among P. syringae pathovars.
    Environ Microbiol. 1999 Feb;1(1):75-87 PMID: 11207720
  29. Complete nucleotide sequence and analysis of pPSR1 (72,601 bp), a pPT23A-family plasmid from Pseudomonas syringae pv. syringae A2.
    Mol Genet Genomics. 2004 Jan;270(6):462-76 PMID: 14634868
  30. Error-prone repair DNA polymerases in prokaryotes and eukaryotes.
    Annu Rev Biochem. 2002;71:17-50 PMID: 12045089
  31. Widespread distribution of a lexA-regulated DNA damage-inducible multiple gene cassette in the Proteobacteria phylum.
    Mol Microbiol. 2004 Oct;54(1):212-22 PMID: 15458417
  32. Growth medium composition-determined regulatory mechanisms are superimposed on CatR-mediated transcription from the pheBA and catBCA promoters in Pseudomonas putida.
    Microbiology. 2001 Aug;147(Pt 8):2149-56 PMID: 11495992
  33. Regulation of the rulAB mutagenic DNA repair operon of Pseudomonas syringae by UV-B (290 to 320 nanometers) radiation and analysis of rulAB-mediated mutability in vitro and in planta.
    J Bacteriol. 2000 Nov;182(21):6137-44 PMID: 11029435
  34. Mutagenesis induced by bacterial UmuDC proteins and their plasmid homologues.
    Mol Microbiol. 1992 Aug;6(16):2213-8 PMID: 1406263
  35. The role of DNA damage in stationary phase ('adaptive') mutation.
    Mutat Res. 1998 Jul;408(1):1-9 PMID: 9678058
  36. 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
  37. Effect of mutY and mutM/fpg-1 mutations on starvation-associated mutation in Escherichia coli: implications for the role of 7,8-dihydro-8-oxoguanine.
    Mol Gen Genet. 1996 Jun 12;251(3):352-7 PMID: 8676878
  38. Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria.
    J Bacteriol. 1990 Nov;172(11):6557-67 PMID: 2172216
  39. The CAM-OCT plasmid enhances UV responses of Pseudomonas aeruginosa recA mutants.
    J Bacteriol. 1990 Mar;172(3):1340-4 PMID: 2106509
  40. New broad-host-range promoter probe vectors based on the plasmid RK2 replicon.
    FEMS Microbiol Lett. 2001 Feb 5;195(1):91-6 PMID: 11167001
  41. Determining mutation rates in bacterial populations.
    Methods. 2000 Jan;20(1):4-17 PMID: 10610800
  42. Effect of degradative plasmid CAM-OCT on responses of Pseudomonas bacteria to UV light.
    J Bacteriol. 1989 Feb;171(2):975-82 PMID: 2914880
  43. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans.
    Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648-52 PMID: 377280
  44. Complete sequence and genetic organization of pDTG1, the 83 kilobase naphthalene degradation plasmid from Pseudomonas putida strain NCIB 9816-4.
    J Mol Biol. 2004 Aug 13;341(3):753-68 PMID: 15288784
  45. 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
  46. Biochemical basis of SOS-induced mutagenesis in Escherichia coli: reconstitution of in vitro lesion bypass dependent on the UmuD'2C mutagenic complex and RecA protein.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9755-60 PMID: 9707548
  47. Sequence diversity of rulA among natural isolates of Pseudomonas syringae and effect on function of rulAB-mediated UV radiation tolerance.
    Appl Environ Microbiol. 2000 Dec;66(12):5167-73 PMID: 11097885
  48. Construction and characterization of new cloning vehicles. II. A multipurpose cloning system.
    Gene. 1977;2(2):95-113 PMID: 344137
  49. Error-prone replication for better or worse.
    Trends Microbiol. 2004 Jun;12(6):288-95 PMID: 15165607
  50. Defining the position of the switches between replicative and bypass DNA polymerases.
    EMBO J. 2004 Oct 27;23(21):4342-52 PMID: 15470496
  51. Complete sequence of the IncP-9 TOL plasmid pWW0 from Pseudomonas putida.
    Environ Microbiol. 2002 Dec;4(12):856-71 PMID: 12534468
  52. cAMP-dependent SOS induction and mutagenesis in resting bacterial populations.
    Proc Natl Acad Sci U S A. 1995 Dec 5;92(25):11736-40 PMID: 8524839
  53. Fate and activity of microorganisms introduced into soil.
    Microbiol Mol Biol Rev. 1997 Jun;61(2):121-35 PMID: 9184007
  54. The SOS response: recent insights into umuDC-dependent mutagenesis and DNA damage tolerance.
    Annu Rev Genet. 2000;34:479-497 PMID: 11092836
  55. Differences in mutagenic and recombinational DNA repair in enterobacteria.
    Proc Natl Acad Sci U S A. 1985 Jun;82(12):4172-6 PMID: 3858873
  56. Microbial competition: Escherichia coli mutants that take over stationary phase cultures.
    Science. 1993 Mar 19;259(5102):1757-60 PMID: 7681219
  57. Autodigestion of lexA and phage lambda repressors.
    Proc Natl Acad Sci U S A. 1984 Mar;81(5):1375-9 PMID: 6231641
  58. The virulence plasmid-encoded impCAB operon enhances survival and induced mutagenesis in Shigella flexneri after exposure to UV radiation.
    Infect Immun. 1999 Mar;67(3):1415-23 PMID: 10024589
  59. Unusual insertion element polymorphisms in the promoter and terminator regions of the mucAB-like genes of R471a and R446b.
    Mutat Res. 1998 Feb 2;397(2):247-62 PMID: 9541650
  60. Nucleotide sequence binding specificity of the LexA repressor of Escherichia coli K-12.
    J Bacteriol. 1985 Jul;163(1):376-84 PMID: 3891738
  61. Comparative genomic analysis of the pPT23A plasmid family of Pseudomonas syringae.
    J Bacteriol. 2005 Mar;187(6):2113-26 PMID: 15743960
  62. Characterization of the Pseudomonas aeruginosa recA analog and its protein product: rec-102 is a mutant allele of the P. aeruginosa PAO recA gene.
    J Bacteriol. 1987 Apr;169(4):1499-508 PMID: 3031014
  63. R plasmids which alter ultraviolet light-sensitivity and enhance ultraviolet light-induced mutability in Pseudomonas aeruginosa.
    J Gen Microbiol. 1978 Sep;108(1):119-23 PMID: 99485
  64. Effect of repair deficiency and R plasmids on spontaneous and radiation-induced mutability in Pseudomonas aeruginosa.
    J Bacteriol. 1979 Sep;139(3):953-60 PMID: 113392
  65. SOS-induced DNA polymerases enhance long-term survival and evolutionary fitness.
    Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8737-41 PMID: 12060704
  66. Mutagenic DNA repair potential in Pseudomonas spp., and characterization of the rulABPc operon from the highly mutable strain Pseudomonas cichorii 302959.
    Can J Microbiol. 2004 Jan;50(1):29-39 PMID: 15052319
  67. Roles of DNA polymerases V and II in SOS-induced error-prone and error-free repair in Escherichia coli.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8350-4 PMID: 11459974
  68. Escherichia coli evolution during stationary phase.
    Res Microbiol. 2004 Jun;155(5):328-36 PMID: 15207864
  69. Improved oligonucleotide site-directed mutagenesis using M13 vectors.
    Nucleic Acids Res. 1985 Jun 25;13(12):4431-43 PMID: 2989795
  70. Resistance to tellurite as a selection marker for genetic manipulations of Pseudomonas strains.
    Appl Environ Microbiol. 1998 Oct;64(10):4040-6 PMID: 9758838
  71. Degradative plasmid TOL provided singlet oxygen resistance for Pseudomonas strains.
    Biochem Biophys Res Commun. 1981 Apr 30;99(4):1245-50 PMID: 7259777
  72. Formation and processing of UV photoproducts: effects of DNA sequence and chromatin environment.
    Photochem Photobiol. 1997 Feb;65(2):270-83 PMID: 9066304
  73. Specialized DNA polymerases, cellular survival, and the genesis of mutations.
    Science. 2002 May 31;296(5573):1627-30 PMID: 12040171
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
DOI
10.1128/JB.187.15.5203-5213.2005
Published
2005-08-00
Pages
5203-13
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC1196032
Subset
IM
External Links
PubMed source DOI: 10.1128/JB.187.15.5203-5213.2005 PMC Full Text View journal details
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