Genetics, Vol. 149, 7-16, May 1998, Copyright © 1998

Single-Strand DNA-Specific Exonucleases in Escherichia coli: Roles in Repair and Mutation Avoidance

Mohan Viswanathana and Susan T. Lovetta
a Department of Biology and Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, Massachusetts 02254-9110

Corresponding author: Susan T. Lovett, Rosenstiel Basic Medical Sciences Center MS029, Brandeis University, Waltham, MA 02254-9110, lovett{at}hydra.rose.brandeis.edu (E-mail).

Communicating editor: L. S. SYMINGTON

Mutations in the genes encoding single-strand DNA-specific exonucleases (ssExos) of Escherichia coli were examined for effects on mutation avoidance, UV repair, and conjugational recombination. Our results indicate complex and partially redundant roles for ssExos in these processes. Although biochemical experiments have implicated RecJ exonuclease, Exonuclease I (ExoI), and Exonuclease VII (ExoVII) in the methyl-directed mismatch repair pathway, the RecJ- ExoI- ExoVII- mutant did not exhibit a mutator phenotype in several assays for base substitution mutations. If these exonucleases do participate in mismatch excision, other exonucleases in E. coli can compensate for their loss. Frameshift mutations, however, were stimulated in the RecJ- ExoI- ExoVII- mutant. For acridine-induced frameshifts, this mutator effect was due to a synergistic effect of ExoI- and ExoVII- mutations, implicating both ExoI and ExoVII in avoidance of frameshift mutations. Although no single exonuclease mutant was especially sensitive to UV irradiation, the RecJ- ExoVII- double mutant was extremely sensitive. The addition of an ExoI- mutation augmented this sensitivity, suggesting that all three exonucleases play partially redundant roles in DNA repair. The ability to inherit genetic markers by conjugation was reduced modestly in the ExoI- RecJ- mutant, implying that the function of either ExoI or RecJ exonucleases enhances RecBCD-dependent homologous recombination.





This article has been cited by other articles:


Home page
MicrobiologyHome page
N. Handa, A. Ichige, and I. Kobayashi
Contribution of RecFOR machinery of homologous recombination to cell survival after loss of a restriction-modification gene complex
Microbiology, July 1, 2009; 155(7): 2320 - 2332.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
V. Palchevskiy and S. E. Finkel
A Role for Single-Stranded Exonucleases in the Use of DNA as a Nutrient
J. Bacteriol., June 1, 2009; 191(11): 3712 - 3716.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
K. Zahradka, M. Buljubasic, M. Petranovic, and D. Zahradka
Roles of ExoI and SbcCD Nucleases in "Reckless" DNA Degradation in recA Mutants of Escherichia coli
J. Bacteriol., March 1, 2009; 191(5): 1677 - 1687.
[Abstract] [Full Text] [PDF]


Home page
MicrobiologyHome page
N. Hulter and W. Wackernagel
Frequent integration of short homologous DNA tracks during Acinetobacter baylyi transformation and influence of transcription and RecJ and SbcCD DNases
Microbiology, December 1, 2008; 154(12): 3676 - 3685.
[Abstract] [Full Text] [PDF]


Home page
Antimicrob. Agents Chemother.Home page
S. Hansen, K. Lewis, and M. Vulic
Role of Global Regulators and Nucleotide Metabolism in Antibiotic Tolerance in Escherichia coli
Antimicrob. Agents Chemother., August 1, 2008; 52(8): 2718 - 2726.
[Abstract] [Full Text] [PDF]


Home page
MutagenesisHome page
J. Serment-Guerrero, M. Brena-Valle, and J. J. Espinosa-Aguirre
In vivo role of Escherichia coli single-strand exonucleases in SOS induction by gamma radiation
Mutagenesis, July 1, 2008; 23(4): 317 - 323.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
B. Thoms, I. Borchers, and W. Wackernagel
Effects of Single-Strand DNases ExoI, RecJ, ExoVII, and SbcCD on Homologous Recombination of recBCD+ Strains of Escherichia coli and Roles of SbcB15 and XonA2 ExoI Mutant Enzymes
J. Bacteriol., January 1, 2008; 190(1): 179 - 192.
[Abstract] [Full Text] [PDF]


Home page
MicrobiologyHome page
E. Kickstein, K. Harms, and W. Wackernagel
Deletions of recBCD or recD influence genetic transformation differently and are lethal together with a recJ deletion in Acinetobacter baylyi
Microbiology, July 1, 2007; 153(7): 2259 - 2270.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
B. E. Dutra, V. A. Sutera Jr., and S. T. Lovett
RecA-independent recombination is efficient but limited by exonucleases
PNAS, January 2, 2007; 104(1): 216 - 221.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. I. Prieto, F. Ramos-Morales, and J. Casadesus
Repair of DNA Damage Induced by Bile Salts in Salmonella enterica
Genetics, October 1, 2006; 174(2): 575 - 584.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
D. Thermic, D. Zahradka, and M. Petranovic
Exonuclease Requirements for Recombination of {lambda}-Phage in recD Mutants of Escherichia coli
Genetics, August 1, 2006; 173(4): 2399 - 2402.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
M. N. Hersh, L. D. Morales, K. J. Ross, and S. M. Rosenberg
Single-Strand-Specific Exonucleases Prevent Frameshift Mutagenesis by Suppressing SOS Induction and the Action of DinB/DNA Polymerase IV in Growing Cells.
J. Bacteriol., April 1, 2006; 188(7): 2336 - 2342.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
D. Thermic
Functions of Multiple Exonucleases Are Essential for Cell Viability, DNA Repair and Homologous Recombination in recD Mutants of Escherichia coli
Genetics, April 1, 2006; 172(4): 2057 - 2069.
[Abstract] [Full Text] [PDF]


Home page
Nucleic Acids ResHome page
E. S. Han, D. L. Cooper, N. S. Persky, V. A. Sutera Jr, R. D. Whitaker, M. L. Montello, and S. T. Lovett
RecJ exonuclease: substrates, products and interaction with SSB
Nucleic Acids Res., February 18, 2006; 34(4): 1084 - 1091.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
N. Sugawara, T. Goldfarb, B. Studamire, E. Alani, and J. E. Haber
Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1
PNAS, June 22, 2004; 101(25): 9315 - 9320.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
A. Miranda and A. Kuzminov
Chromosomal Lesion Suppression and Removal in Escherichia coli via Linear DNA Degradation
Genetics, April 1, 2003; 163(4): 1255 - 1271.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
V. V. Feschenko, L. A. Rajman, and S. T. Lovett
Stabilization of perfect and imperfect tandem repeats by single-strand DNA exonucleases
PNAS, February 4, 2003; 100(3): 1134 - 1139.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
D. Zahradka, K. Zahradka, M. Petranovic, D. Dermic, and K. Brcic-Kostic
The RuvABC Resolvase Is Indispensable for Recombinational Repair in sbcB15 Mutants of Escherichia coli
J. Bacteriol., August 1, 2002; 184(15): 4141 - 4147.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
E. P. Skaar, M. P. Lazio, and H. S. Seifert
Roles of the recJ and recN Genes in Homologous Recombination and DNA Repair Pathways of Neisseria gonorrhoeae
J. Bacteriol., February 15, 2002; 184(4): 919 - 927.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
D. A. Cano, M. G. Pucciarelli, F. Garcia-del Portillo, and J. Casadesus
Role of the RecBCD Recombination Pathway in Salmonella Virulence
J. Bacteriol., January 15, 2002; 184(2): 592 - 595.
[Abstract] [Full Text] [PDF]


Home page
Mol. Cell. Biol.Home page
N. S. Amin, M.-N. Nguyen, S. Oh, and R. D. Kolodner
exo1-Dependent Mutator Mutations: Model System for Studying Functional Interactions in Mismatch Repair
Mol. Cell. Biol., August 1, 2001; 21(15): 5142 - 5155.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
V. Burdett, C. Baitinger, M. Viswanathan, S. T. Lovett, and P. Modrich
In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair
PNAS, May 24, 2001; (2001) 121183298.
[Abstract] [Full Text] [PDF]


Home page
Nucleic Acids ResHome page
A. Yamamoto, M. J. Schofield, I. Biswas, and P. Hsieh
Requirement for Phe36 for DNA binding and mismatch repair by Escherichia coli MutS protein
Nucleic Acids Res., September 15, 2000; 28(18): 3564 - 3569.
[Abstract] [Full Text] [PDF]


Home page
Mol. Cell. Biol.Home page
P. T. Tran and R. M. Liskay
Functional Studies on the Candidate ATPase Domains of Saccharomyces cerevisiae MutLalpha
Mol. Cell. Biol., September 1, 2000; 20(17): 6390 - 6398.
[Abstract] [Full Text]


Home page
MicrobiologyHome page
J. M. Dow, J.-X. Feng, C. E. Barber, J.-L. Tang, and M. J. Daniels
Novel genes involved in the regulation of pathogenicity factor production within the rpf gene cluster of Xanthomonas campestris
Microbiology, April 1, 2000; 146(4): 885 - 891.
[Abstract] [Full Text]


Home page
J. Bacteriol.Home page
R. Friedman-Ohana, I. Karunker, and A. Cohen
A RecG-Independent Nonconservative Branch Migration Mechanism in Escherichia coli Recombination
J. Bacteriol., December 1, 1999; 181(23): 7199 - 7205.
[Abstract] [Full Text]


Home page
GeneticsHome page
Y.-J. Huang, M. M. Parker, and M. Belfort
Role of Exonucleolytic Degradation in Group I Intron Homing in Phage T4
Genetics, December 1, 1999; 153(4): 1501 - 1512.
[Abstract] [Full Text]


Home page
J. Biol. Chem.Home page
M. Viswanathan and S. T. Lovett
Exonuclease X of Escherichia coli. A NOVEL 3'-5' DNase AND DnaQ SUPERFAMILY MEMBER INVOLVED IN DNA REPAIR
J. Biol. Chem., October 15, 1999; 274(42): 30094 - 30100.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
G. T. Marsischky and R. D. Kolodner
Biochemical Characterization of the Interaction between the Saccharomyces cerevisiae MSH2-MSH6 Complex and Mispaired Bases in DNA
J. Biol. Chem., September 17, 1999; 274(38): 26668 - 26682.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
P. L. Foster and W. A. Rosche
Increased Episomal Replication Accounts for the High Rate of Adaptive Mutation in recD Mutants of Escherichia coli
Genetics, May 1, 1999; 152(1): 15 - 30.
[Abstract] [Full Text]


Home page
Mol. Cell. Biol.Home page
H. T. Tran, D. A. Gordenin, and M. A. Resnick
The 3'right-arrow5' Exonucleases of DNA Polymerases delta  and varepsilon  and the 5'right-arrow3' Exonuclease Exo1 Have Major Roles in Postreplication Mutation Avoidance in Saccharomyces cerevisiae
Mol. Cell. Biol., March 1, 1999; 19(3): 2000 - 2007.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
M. Viswanathan, A. Lanjuin, and S. T. Lovett
Identification of RNase T as a High-Copy Suppressor of the UV Sensitivity Associated With Single-Strand DNA Exonuclease Deficiency in Escherichia coli
Genetics, March 1, 1999; 151(3): 929 - 934.
[Abstract] [Full Text]


Home page
J. Biol. Chem.Home page
M. Viswanathan, K. W. Dower, and S. T. Lovett
Identification of a Potent DNase Activity Associated with RNase T of Escherichia coli
J. Biol. Chem., December 25, 1998; 273(52): 35126 - 35131.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
H. Flores-Rozas and R. D. Kolodner
The Saccharomyces cerevisiae MLH3 gene functions in MSH3-dependent suppression of frameshift mutations
PNAS, October 13, 1998; 95(21): 12404 - 12409.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
D. J. Mazur and F. W. Perrino
Excision of 3' Termini by the Trex1 and TREX2 3'right-arrow5' Exonucleases. CHARACTERIZATION OF THE RECOMBINANT PROTEINS
J. Biol. Chem., May 11, 2001; 276(20): 17022 - 17029.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
C. Schmutte, M. M. Sadoff, K.-S. Shim, S. Acharya, and R. Fishel
The Interaction of DNA Mismatch Repair Proteins with Human Exonuclease I
J. Biol. Chem., August 31, 2001; 276(35): 33011 - 33018.
[Abstract] [Full Text] [PDF]


Home page
J. Biol. Chem.Home page
M. Viswanathan, V. Burdett, C. Baitinger, P. Modrich, and S. T. Lovett
Redundant Exonuclease Involvement in Escherichia coli Methyl-directed Mismatch Repair
J. Biol. Chem., August 10, 2001; 276(33): 31053 - 31058.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
V. Burdett, C. Baitinger, M. Viswanathan, S. T. Lovett, and P. Modrich
In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair
PNAS, June 5, 2001; 98(12): 6765 - 6770.
[Abstract] [Full Text] [PDF]