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Journal of Bacteriology, March 2006, p. 2285-2289, Vol. 188, No. 6
0021-9193/06/$08.00+0     doi:10.1128/JB.188.6.2285-2289.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

YtkD and MutT Protect Vegetative Cells but Not Spores of Bacillus subtilis from Oxidative Stress

Francisco X. Castellanos-Juárez,¹ Carlos Álvarez-Álvarez,¹ Ronald E. Yasbin,³ Barbara Setlow,² Peter Setlow,² and Mario Pedraza-Reyes^1*

Institute of Investigation in Experimental Biology, Faculty of Chemistry, University of Guanajuato, P.O. Box 187, Guanajuato, Gto. 36050, Mexico,¹ Department of Molecular, Microbial and Structural Biology, University of Connecticut Health Center, Farmington, Connecticut 06032,² Department of Biology, University of Nevada—Las Vegas, 4505 Maryland Parkway, Box 454001, Las Vegas, Nevada 89154-9900³

Received 29 August 2005/ Accepted 4 January 2006

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ytkD and mutT of Bacillus subtilis encode potential 8-oxo-dGTPases that can prevent the mutagenic effects of 8-oxo-dGTP. Loss of YtkD but not of MutT increased the spontaneous mutation frequency of growing cells. However, cells lacking both YtkD and MutT had a higher spontaneous mutation frequency than cells lacking YtkD. Loss of either YtkD or MutT sensitized growing cells to hydrogen peroxide (H₂O₂) and t-butylhydroperoxide (t-BHP), and the lack of both proteins sensitized growing cells to these agents even more. In contrast, B. subtilis spores lacking YtkD and MutT were not sensitized to H₂O₂, t-BHP, or heat. These results suggest (i) that YtkD and MutT play an antimutator role and protect growing cells of B. subtilis against oxidizing agents, and (ii) that neither YtkD nor MutT protects spores against potential DNA damage induced by oxidative stress or heat.

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Endogenous reactive oxygen species (ROS), such as the superoxide radical, hydrogen peroxide (H₂O₂), and the hydroxyl radical (OH·), are generated as byproducts of cellular metabolism (33, 34). These ROS can react with proteins, lipids, and DNA (18, 20, 31), generating both cytotoxic and genotoxic effects (4). OH· can oxidize dGTP to 8-oxo-dGTP, which is frequently incorporated opposite adenine in DNA (20), and oxidation of guanines in DNA also generates 8-oxo-G, which induces GCTA and ATCG transversions (35). 8-Oxo-G and other oxidized bases are also a potential source of other DNA lesions, such as apurinic/apyrimidinic (AP) sites, sites of sugar damage, and single and double strand breaks (5).

The mutagenic effects of 8-oxo-G are counteracted in Escherichia coli by the base excision repair pathway utilizing the DNA glycosylases MutM and MutY (13). The former releases 8-oxo-G from 8-oxo-G:C pairs, and the latter removes adenine from 8-oxo-G:A mispairs (13). The mutagenic effects of 8-oxo-dGTP are also prevented by MutT, which hydrolyzes this triphosphate to the monophosphate, blocking 8-oxo-G incorporation into DNA (9). The contributions of MutM, MutY, and MutT greatly reduce the mutagenic effects of 8-oxo-G in E. coli, and together these proteins make up the oxidized guanine (GO) system (5).

It was recently reported that ytkD of Bacillus subtilis, which encodes an 8-oxo-dGTPase, partially complemented the mutagenic phenotype of a mutT E. coli strain (17). In B. subtilis, ytkD is transcribed both during vegetative growth and during sporulation by RNA polymerases containing ^A and ^F, respectively (17). This pattern of ytkD expression suggests that YtkD may have some function in both vegetative cells and spores of B. subtilis. In addition to ytkD, there is a second B. subtilis gene termed mutT that also encodes a putative 8-oxo-dGTPase (8), but the biochemical properties and physiological function of MutT are unknown. B. subtilis seems to contain a complete GO system, since its genome also has mutM and yfhQ genes that encode potential homologs of E. coli MutM and MutY, respectively (21).

In order to investigate the role played by YtkD and MutT in protecting growing cells and spores of B. subtilis from the toxic effects of ROS, we constructed single and double ytkD and mutT mutants. Our results revealed that inactivation of ytkD conferred a mutagenic phenotype on B. subtilis cells, and this phenotype is exacerbated when combined with a mutT mutation. In agreement with these results, growing cells of B. subtilis lacking YtkD, MutT, or both proteins were more sensitive to oxidizing agents than growing cells of the wild-type strain were. However, YtkD and MutT had no role in protecting B. subtilis spores against oxidizing agents and heat.

YtkD and MutT protect growing cells against oxidizing agents. To investigate the physiological role played by ytkD and mutT in B. subtilis, strains with single or double knockout mutations in these genes were constructed. To this end, plasmids pPERM590, containing the ytkD gene interrupted by a neomycin resistance cassette, and pPERM594, containing the mutT gene interrupted by a tetracycline resistance cassette (Table 1), were designed and amplified in E. coli (19). Plasmids pPERM590 and pPERM594 were used to transform B. subtilis strains PS832 (wild type) and PS356 (^–ß^–, i.e., lacking most of the spore's DNA protective /ß-type small, acid-soluble spore proteins [SASP]), generating strains PERM595 (ytkD), PERM596 (mutT), PERM604 (^–ß^– ytkD), and PERM605 (^–ß^– mutT) (Table 1). The ytkD mutT strains in the PS832 and PS356 backgrounds were generated by transforming strains PERM595 and PERM604 with plasmid pPERM594, giving strains PERM597 (mutT ytkD) and PERM606 (^–ß^– mutT ytkD). The double crossover events leading to the inactivation of the appropriate genes were confirmed by PCR (data not shown).

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TABLE 1. Strains and plasmids used in this work

It has been previously suggested that YtkD plays an antimutator role in B. subtilis (17). Indeed, a ytkD mutant did have an increased mutation frequency to rifampin resistance (Rif^r) with respect to the value for the isogenic wild-type strain (Fig. 1A). However, inactivation of ytkD increased the mutation frequency of B. subtilis cells only 4-fold (Fig. 1A), suggesting that proteins with similar functions are present in this microorganism. In addition to ytkD, the B. subtilis genome contains a second gene that may also encode an 8-oxo-dGTPase, mutT (8). Although disruption of mutT alone did not generate a mutator phenotype (Fig. 1A), the introduction of a mutT mutation into the ytkD strain significantly increased the mutation frequency (Fig. 1A). Treatment of the mutT ytkD strain with 25 mM H₂O₂ also caused a twofold increase in its mutation frequency (Fig. 1B). Previous results revealed that ytkD from B. subtilis partially reversed the mutagenic effect of a mutT mutation in E. coli, suggesting that YtkD also protects B. subtilis cells against the mutagenic effects of 8-oxo-dGTP (17). These results appear to be correct, since a B. subtilis ytkD disruptant had a significantly higher spontaneous mutation frequency than the wild-type parental strain. A recent study showed that independent or simultaneous disruption of mutT, yjhB, and yvcI, which encode three potential MutT homologs, did not increase the spontaneous mutation frequency of B. subtilis, suggesting either that none of these genes encode 8-oxo-dGTPases or that the gene products are important only under special circumstances (21). Therefore, ytkD is the only mutT homolog whose single disruption causes a significant mutator phenotype in B. subtilis. Our results confirmed that a mutT mutant of B. subtilis did not exhibit a mutator phenotype. However, there was a small but significant increase in the mutation frequency of the mutT ytkD strain over that of the ytkD strain. These results suggest that MutT may have a slight antimutator role in B. subtilis and that YtkD and MutT may function in a cooperative manner. However, in contrast to what was seen for E. coli (9), the inactivation of ytkD alone or in combination with mutT did not confer a strong mutator phenotype to B. subtilis. Therefore, either B. subtilis relies on proteins in addition to YtkD and MutT to hydrolyze oxidized nucleotides or the combined action of YtkD, MutT, and the DNA glycosylases MutM and YfhQ is sufficient to counteract the mutagenic effects induced by these potentially mutagenic precursors.

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FIG. 1. (A) Spontaneous mutation frequencies of wild-type, ytkD, mutT, and mutT ytkD B. subtilis strains. Cells were grown for 12 h at 37°C in PB (antibiotic 3; Difco) medium supplemented with the proper antibiotics, and aliquots were plated on six LB plates (14) containing 10 µg/ml rifampin. Rifr colonies were counted after 1 day of incubation at 37°C. Values shown represent averages of three independent experiments ± standard deviations. (B) Spontaneous mutation frequencies of wild-type and mutT ytkD B. subtilis strains in the presence or absence of 25 mM H2O2. Cells were grown at 37°C in PB medium to an OD600 of 0.5 and then divided in two Erlenmeyer flasks; one of the flasks was supplemented with 25 mM H2O2. Cultures were shaken for 2.5 h at 37°C, and aliquots were plated on six LB plates containing 10 µg/ml rifampin. Rifr colonies were counted after 1 day of incubation at 37°C. Values shown represent averages of three independent experiments ± standard deviations. WT, wild type.

We further investigated whether ytkD and mutT participate in counteracting the adverse effects of oxidizing agents during vegetative growth. Strains lacking YtkD, MutT, or both proteins were grown to mid-logarithmic phase and treated with different concentrations of H₂O₂ for 2 h, and cell viability was measured (Fig. 2A). The ytkD and mutT strains were killed more rapidly when incubated with H₂O₂ at concentrations up to 25 mM than the wild-type strain was (Fig. 2A). The optical density at 600 nm (OD₆₀₀) of the single mutant strains treated with higher H₂O₂ concentrations also fell significantly more than did the OD₆₀₀ of the wild-type strain (data not shown). Loss of both mutT and ytkD further increased cell sensitivity to H₂O₂ (Fig. 2A). The lack of either YtkD or MutT also slightly increased B. subtilis cell sensitivity to t-BHP (Fig. 2B). The lack of both enzymes rendered B. subtilis cells very sensitive to increasing concentrations of t-BHP (Fig. 2B). Therefore, one of the most important conclusions derived from this work is that YtkD and MutT protect B. subtilis cells from the adverse effects of H₂O₂ and t-BHP. Although mutation of either ytkD or mutT sensitized B. subtilis cells to hydrogen peroxide and t-BHP, the loss of both genes considerably increased the sensitivity of cells to these DNA-damaging agents. In addition, hydrogen peroxide increased the mutation frequency of a mutT ytkD mutant (Fig. 1B). Therefore, these results are consistent with the notion that YtkD and MutT function in the same cellular pathway, presumably via hydrolysis of the mutagenic nucleic acid precursor 8-oxo-dGTP (17). However, more work is needed to prove this hypothesis, especially for MutT.

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FIG. 2. Resistance of wild-type, ytkD, mutT, and mutT ytkD cells to H2O2 (A) or t-BHP (B). Strains were grown overnight at 37°C in LB medium containing the appropriate antibiotics and diluted (1:50) into fresh PB medium. These cultures were grown at 37°C to an OD600 of 1.0, treated with different concentrations of H2O2 or t-BHP, and incubated for 2 h at 37°C with shaking. Cell suspensions were diluted in phosphate-buffered saline (pH 7.4) (16), and aliquots were plated on solid LB medium containing the appropriate antibiotics. Colonies were counted after 1 to 2 days of incubation at 37°C, and results were plotted as averages of three independent experiments ± standard deviations. The symbols for the strains used are as follows: •, PS832 (wild type); , PERM595 (ytkD); , PERM596 (mutT); and , PERM597 (mutT ytkD).

Properties of mutT and ytkD B. subtilis spores. Since growing cells of B. subtilis lacking ytkD and mutT were sensitive to H₂O₂ and t-BHP, we examined the effect of ytkD and mutT mutations on spore resistance to these agents. The resistance of mutT ytkD spores to heat was also examined, since it has been suggested that heat may kill spores by oxidative damage caused by free radicals (10). However, the resistance of mutT ytkD spores to H₂O₂, t-BHP, wet heat, or dry heat was indistinguishable from that of spores of the wild-type parental strain (Table 2).

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TABLE 2. Resistance of wild-type and mutant spores of B. subtilis to various treatmentsa

Spores lacking the two major DNA protective /ß-type SASP (termed ^–ß^– spores) are significantly more susceptible to oxidizing chemicals and other DNA damaging agents than are wild-type spores (12, 25, 28, 30). As expected, ^–ß^– spores were considerably more sensitive to H₂O₂, t-BHP, and wet and dry heat than spores of the wild-type strain (Table 2). However, a ytkD mutation had no effect on the resistance of ^–ß^– spores to heat, H₂O₂, or t-BHP, nor did the mutT ytkD double mutation (Table 2).

A recent study showed that ytkD is transcribed both during vegetative growth and within the developing forespore (17). This suggested that YtkD could play a role in protecting spores from DNA damage by free radicals (17). However, in contrast to the clear phenotypes of the mutT, yktD, and mutT yktD mutations in growing cells, inactivation of ytkD and mutT did not sensitize spores to H₂O₂, t-BHP, or wet or dry heat. There are a number of reasons why B. subtilis spores might not require YtkD, MutT, and other proteins of the GO system to counteract the damaging effects of oxidizing agents. For wild-type spores, the main reason is likely the protection conferred on DNA by its saturation with /ß-type SASP, as oxidizing agents do not kill wild-type spores via DNA damage (23). There is also evidence that wet heat killing of spores does not occur through oxidative damage, since this type of treatment did not increase the number of oxidized and ring-opened guanines in spore DNA (29).

As noted above, the /ß-type SASP are very important in protecting spore DNA from damage caused by wet and dry heat, UV radiation, lyophilization, and a number of genotoxic chemicals (15, 28, 30). However, ^–ß^– spores deficient in YtkD and MutT were not sensitized to oxidizing agents or heat. Thus, is very possible that MutT and YtkD do not have a role in protecting dormant spores against oxidizing agents, as spores of Bacillus species have insignificant levels of nucleoside triphosphates (27, 29). Therefore, even a full GO system would not be operative in spores, as spores cannot accumulate 8-oxo-dGTP or incorporate this modified nucleotide into DNA.

On the other hand, dormant spores do contain significant levels of GMP that may be converted to 8-oxo-GTP in the first minutes of spore outgrowth (27). This nucleotide not only may be incorporated into RNA but also may be a precursor for the synthesis of 8-oxo-dGTP when deoxynucleotide triphosphates are accumulated early in spore outgrowth to allow DNA repair synthesis to take place, a process followed later by DNA replication (26, 27). Consequently, it was possible that YtkD and MutT as well as other components of the GO repair synthesis could be required to protect outgrowing spores against ROS. To test this notion, wild-type and mutT ytkD spores were heat shocked (30 min at 70°C) and then germinated at an OD₆₀₀ of 0.5 to 0.7 in LB medium supplemented with 4 mM L-alanine (16) in the presence of 0.2 or 2 mM H₂O₂ added 15 min after the initiation of germination or in the absence of H₂O₂ (2)_. Analysis of the OD₆₀₀ and viable counts over the next 240 min revealed that, as previously described (2), H₂O₂ at 0.2 mM had no effect on the outgrowth and resumption of vegetative growth of wild-type spores, but 2 mM of the oxidizing agent slowed the return to vegetative growth of this strain (data not shown). However, inactivation of YtkD and MutT did not increase the sensitivity of the germinating and outgrowing spores to these concentrations of H₂O₂ (data not shown). Therefore, these results suggest that additional factors, such as KatX (2) and perhaps MutY and MutM, are sufficient to protect the germinating spore from the genotoxic effects of ROS.

 
This work was supported by grant 43644 from the Consejo Nacional de Ciencia y Tecnología (CONACYT) of México to M. Pedraza-Reyes. F. X. Castellanos-Juárez and C. Álvarez-Álvarez were supported by fellowships from CONACYT. B. Setlow and P. Setlow were supported by grants from the Army Research Office and the National Institutes of Health (GM19698). R. E. Yasbin was supported by MCB-0317076 from the National Science Foundation.

We thank A. Ibarra for technical assistance.

 
* Corresponding author. Mailing address: Institute of Investigation in Experimental Biology, Building L, Faculty of Chemistry, University of Guanajuato, Noria Alta S/N, Guanajuato, 36050 Gto., Mexico. Phone: (473) 73 2 00 06, ext. 8161. Fax: (473) 73 2 00 06, ext. 8153. E-mail: pedrama{at}quijote.ugto.mx.

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1
1. Boylan, R. J., N. H. Mendelson, D. Brooks, and F. E. Young. 1972. Regulation of the bacterial cell wall: analysis of a mutant of Bacillus subtilis defective in the biosynthesis of teichoic acid. J. Bacteriol. 173:281-290.
2
2. Casillas-Martinez, L., and P. Setlow. 1997. Alkyl hydroperoxide reductase, catalase, MrgA, and superoxide dismutase are not involved in resistance of Bacillus subtilis spores to heat or oxidizing agents. J. Bacteriol. 179:7420-7425.[Abstract/Free Full Text]
3
3. Cutting, S. M., and P. B. Vander Horn. 1990. Genetic analysis, p. 27-74. In C. R. Harwood and S. M. Cutting (ed.), Molecular biological methods for Bacillus. John Wiley and Sons, Sussex, England.
4
4. Demple, B., and L. Harrison. 1994. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63:915-948.[CrossRef][Medline]
5
5. Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA repair and mutagenesis. American Society for Microbiology, Washington D.C.
6
6. Guérout-Fleury, A. M., K. Shazand, N. Frandsen, and P. Stragier. 1995. Antibiotic-resistance cassettes for Bacillus subtilis. Gene 167:335-336.[CrossRef][Medline]
7
7. Itaya, M., K. Kondo, and T. Tanaka. 1989. A neomycin resistance gene cassette selectable in a single copy state in Bacillus subtilis. Nucleic Acids Res. 17:4410.[Free Full Text]
8
8. Kunst, F., N. Ogasawara, I. Moszer, A. M. Albertini, G. Alloni, V. Azevedo, M. G. Bertero, P. Bessieres, A. Bolotin, S. Borchert, R. Borriss, L. Boursier, A. Brans, M. Braun, S. C. Brignell, S. Bron, S. Brouillet, C. V. Bruschi, B. Caldwell, V. Capuano, N. M. Carter, S. K. Choi, J. J. Codani, I. F. Conerton, A. Danchin, et al. 1997. The complete genome sequence of the Gram positive bacterium Bacillus subtilis. Nature 390:249-256.[CrossRef][Medline]
9
9. Maki, H., and M. Sekiguchi. 1992. MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355:273-275.[CrossRef][Medline]
10
10. Marquis, R. E., J. Sim, and S. Y. Shin. 1994. Molecular mechanisms of resistance to heat and oxidative damage. J. Appl. Bacteriol. 76:40S-48S.
11
11. Mason, J. M., and P. Setlow. 1986. Essential role of small, acid-soluble spore proteins in resistance of Bacillus subtilis spores to ultraviolet light. J. Bacteriol. 167:174-178.[Abstract/Free Full Text]
12
12. Melly, E., A. E. Cowan, and P. Setlow. 2002. Studies on the mechanism of killing of Bacillus subtilis spores by hydrogen peroxide. J. Appl. Microbiol. 93:316-325.[CrossRef][Medline]
13
13. Michaels, M., and J. H. Miller. 1992. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J. Bacteriol. 174:6321-6325.[Free Full Text]
14
14. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
15
15. Nicholson, W. L., N. Munakata, G. Horneck, H. G. Melosh, and P. Setlow. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiol. Mol. Biol. Rev. 64:548-572.[Abstract/Free Full Text]
16
16. Nicholson, W. L., and P. Setlow. 1990. Sporulation, germination and outgrowth, p. 391-450. In C. R. Harwood and S. M. Cutting (ed.), Molecular biological methods for Bacillus. John Wiley and Sons, Sussex, England.
17
17. Ramírez, M. I., F. X. Castellanos-Juárez, R. E. Yasbin, and M. Pedraza-Reyes. 2004. The ytkD (mutTA) gene of Bacillus subtilis encodes a functional antimutator 8-oxo (dGTP/GTP)ase and is under dual control of sigma A and sigma F RNA polymerases. J. Bacteriol. 186:1050-1059.[Abstract/Free Full Text]
18
18. Riley, P. A. 1994. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int. J. Radiat. Biol. 65:27-37.[Medline]
19
19. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
20
20. Saran, M., and W. Bors. 1990. Radical reactions in vivo—an overview. Radiat. Environ. Biophys. 29:249-262.[CrossRef][Medline]
21
21. Sasaki, M., Y. Yonemura, and Y. Kurusu. 2000. Genetic analysis of Bacillus subtilis mutator genes. J. Gen. Appl. Microbiol. 46:183-187.
22
22. Schaeffer, P., J. Millet, and J. P. Aubert. 1965. Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. USA 54:704-711.[Free Full Text]
23
23. Setlow, B., C. Setlow, and P. Setlow. 1997. Killing bacterial spores by organic hydroperoxides. J. Ind. Microbiol. 18:384-388.[CrossRef]
24
24. Setlow, B., and P. Setlow. 1993. Binding of small, acid-soluble spore proteins to DNA plays a significant role in the resistance of Bacillus subtilis spores to hydrogen peroxide. Appl. Environ. Microbiol. 59:3418-3423.[Abstract/Free Full Text]
25
25. Setlow, B., and P. Setlow. 1994. Heat inactivation of Bacillus subtilis spores lacking small, acid-soluble spore proteins is accompanied by generation of abasic sites in spore DNA. J. Bacteriol. 176:2111-2113.[Abstract/Free Full Text]
26
26. Setlow, B., and P. Setlow. 1996. Role of DNA repair in Bacillus subtilis spore resistance. J. Bacteriol. 178:3486-3495.[Abstract/Free Full Text]
27
27. Setlow, P. 1973. Deoxyribonucleic acid synthesis and deoxynucleotide metabolism during bacterial spore germination. J. Bacteriol. 114:1099-1107.[Abstract/Free Full Text]
28
28. Setlow, P. 1988. Small acid-soluble spore proteins of Bacillus species: structure, synthesis, genetics, function and degradation. Annu. Rev. Microbiol. 42:319-338.[CrossRef][Medline]
29
29. Setlow, P. 1994. Mechanisms which contribute to the long-term survival of spores of Bacillus species. J. Appl. Bacteriol. 23:49S-60S.
30
30. Setlow, P. 1995. Mechanisms for the prevention of damage to the DNA in spores of Bacillus species. Annu. Rev. Microbiol. 49:29-54.[CrossRef][Medline]
31
31. Simic, M. G., K. A. Taylor, J. F. Ward, and C. Von Sonntag (ed.). 1988. Basic life sciences, vol. 49. Oxygen radicals in biology and medicine. Plenum Publishing Corp., New York, N.Y.
32
32. Spizizen, J. 1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc. Natl. Acad. Sci. USA 44:1072-1078.[Free Full Text]
33
33. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.[CrossRef][Medline]
34
34. Storz, G., and M. Zheng. 2000. Oxidative stress. p. 47-59. In G. Storz and R. Hengge-Aronis (ed.), Bacterial stress responses. ASM Press, Washington, D.C.
35
35. Tajiri, T., H. Maki, and M. Sekiguchi. 1995. Functional cooperation of MutT, MutM and MutY proteins in preventing mutations caused by spontaneous oxidation of guanine nucleotide in Escherichia coli. Mutat. Res. 336:257-267.[Medline]

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Journal of Bacteriology, March 2006, p. 2285-2289, Vol. 188, No. 6
0021-9193/06/$08.00+0     doi:10.1128/JB.188.6.2285-2289.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

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