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Journal of Bacteriology, June 2005, p. 3693-3697, Vol. 187, No. 11
0021-9193/05/$08.00+0     doi:10.1128/JB.187.11.3693-3697.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Characterization of Pathways Dependent on the uvsE, uvrA1, or uvrA2 Gene Product for UV Resistance in Deinococcus radiodurans

Masashi Tanaka,^1,2, Issay Narumi,² Tomoo Funayama,² Masahiro Kikuchi,² Hiroshi Watanabe,² Tsukasa Matsunaga,³ Osamu Nikaido,³ and Kazuo Yamamoto^1,2*

Department of Biomolecular Sciences, Graduate School of Life Sciences, Tohoku University, Sendai 980-8577,¹ Research Group for Biotechnology Development, Takasaki Radiation Chemistry Research Establishment, Japan Atomic Energy Research Institute, Takasaki 370-1292,² Laboratory of Molecular Human Genetics, Faculty of Pharmaceutical Sciences, Kanazawa University, Kanazawa 920-0934, Japan³

Received 4 February 2005/ Accepted 1 March 2005

Top Abstract Introduction Materials and Methods Results Discussion References

 
The genome of a radiation-resistant bacterium, Deinococcus radiodurans, contains one uvsE gene and two uvrA genes, uvrA1 and uvrA2. Using a series of mutants lacking these genes, we determined the biological significance of these components to UV resistance. The UV damage endonuclease (UvsE)-dependent excision repair (UVER) pathway and UvrA1-dependent pathway show some redundancy in their function to counteract the lethal effects of UV. Loss of these pathways does not cause increased sensitivity to UV mutagenesis, suggesting either that these pathways play no function in inducing mutations or that there are mechanisms to prevent mutation other than these excision repair pathways. UVER efficiently removes both cyclobutane pyrimidine dimers (CPDs) and pyrimidine (6-4) pyrimidone photoproducts (6-4PPs) from genomic DNA. In contrast, the UvrA1 pathway does not significantly contribute to the repair of CPDs but eliminates 6-4PPs. Inactivation of uvrA2 does not result in a deleterious effect on survival, mutagenesis, or the repair kinetics of CPDs and 6-4PPs, indicating a minor role in resistance to UV. Loss of uvsE, uvrA1, and uvrA2 reduces but does not completely abolish the ability to eliminate CPDs and 6-4PPs from genomic DNA. The result indicates the existence of a system that removes UV damage yet to be identified.

Top Abstract Introduction Materials and Methods Results Discussion References

 
UV light damages DNA, generating cyclobutane pyrimidine dimers (CPDs) and pyrimidine (6-4) pyrimidone photoproducts (6-4PPs) (3). The biological consequences of this are severe because these two major UV photoproducts interfere with the functions of the DNA replication and transcription machinery. Therefore, organisms have had to develop mechanisms to deal with these lesions during evolution. A radiation-resistant bacterium, Deinococcus radiodurans, exhibits extreme resistance to UV, being about 20 times more resistant than Escherichia coli (15). This has led to the notion that D. radiodurans possesses highly efficient mechanisms to recover from UV-induced damage. The Deinococcus genome contains uvsE, uvrA1, and uvrA2 genes, which may encode proteins that contribute to the resistance to UV, whereas homologues of phr, flap endonuclease (FEN), and translesion synthesis (TLS) polymerase have not been identified (15). This suggests several possibilities in terms of resistance to UV. The first is that D. radiodurans has evolved UV damage endonuclease (UvsE)-dependent excision repair (UVER) as an alternative pathway to photoreactivation, although the subsequent process likely depends on a different mechanism from that associated with flap endonuclease (17). The second possibility is that two different UvrA proteins are involved in nucleotide excision repair (NER) in D. radiodurans. Also, the possible lack of TLS suggests the presence of unique mechanisms to overcome a situation in which the replication fork is stalled at the site damaged by UV.

Recently, it was reported that loss of uvsE in the uvrA1 background sensitizes the Deinococcus strain to UV (2). The result indicates that as in Schizosaccharomyces pombe, the NER and UVER pathways possess a redundant function in the recovery from UV damage in D. radiodurans (2, 17). However, it remains unclear which mechanisms play a major role in resistance to UV in D. radiodurans, because the deinococcal ability to remove lesions from the genomic DNA and its biological significance in this species have not been elucidated. To determine the capacity of UVER and NER to eliminate CPDs and 6-4PPs and a possible role of UvrA2 in UV resistance, we examined the sensitivities and repair kinetics of a series of mutants lacking uvsE, uvrA1, and/or uvrA2. We also analyzed the survival of strains deficient in excision repair pathways or homologous recombination (HR) to determine the relative contributions of these pathways to UV resistance. Here we provide evidence that (i) UvrA2 plays a minor role in UV resistance, (ii) UVER eliminates both CPDs and 6-4PPs, (iii) NER removes 6-4PPs but does not significantly contribute to the repair of CPDs, and (iv) HR plays a more significant role than UVER or NER in the resistance to UV.

Top Abstract Introduction Materials and Methods Results Discussion References

 
Strains and growth conditions. Strains used in this study are listed in Table 1. All strains derived from D. radiodurans MR₁ were grown at 30°C in TGY broth (0.5% tryptone, 0.3% yeast extract, and 0.1% glucose) or on TGY plate (1.5% agar) (3). E. coli strains were grown at 37°C in Luria-Bertani (LB) broth or on LB agar.

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TABLE 1. Strains used in this study

Measurement of survival rate and mutation frequency. D. radiodurans cultures in the early stationary phase were washed twice with phosphate buffered saline (PBS) containing 0.02% Triton X-100 to ensure the separation of individual CFU, resuspended in PBS, and used for UV exposure. UV irradiation was conducted using a germicidal lamp (GL-15; Matsushita, Osaka, Japan) at a rate of 2.3 J/m²/s. Survival was determined by plating serial dilutions of irradiated cells on TGY plates and incubating at 30°C for 3 days. Strain TNK007 was scored 4 days after plating. For mutation experiments, UV-irradiated strain MR₁ (1,500 J/m²) and UV-irradiated strains TNK003 and TNK006 (120 J/m²) were inoculated on TGY plates and incubated for 3 days to fix the mutation. Cultures were harvested and suspended in PBS containing 0.02% Triton X-100. Serial dilutions with PBS were plated onto TGY plates containing 50 µg/ml rifampin (Rif) and incubated for 4 days before scoring. The total number of CFU was determined by plating serial dilutions on TGY plates. The frequency of mutation conferring resistance to Rif was determined as the ratio of mutant bacteria on Rif plates to total viable bacteria on TGY plates.

Construction of strains. Gene disruption was performed by targeted mutagenesis as described previously (4). To create strain TNK001, a 3.6-kbp genomic DNA fragment containing the uvsE gene, encoding UV damage endonuclease, was cloned into pBS (SK+) at AccI and EcoRI sites, generating pTNK001. This plasmid was digested with HindIII and SphI (these restriction sites are located in the uvsE gene) and ligated with a 0.8-kbp fragment from pKatAAD, a streptomycin-resistant version of pKatCAT (4). The resulting plasmid was designated pTNK002. The uvsE disruption plasmid was introduced into D. radiodurans MR₁, and the recombinants were selected on TGY plates containing 8 µg/ml streptomycin. The disruption of uvsE was confirmed by PCR using 5'-TGGCGTAAGAAATGGGAGCGCGA-3' and 5'-CAGTCGTCAGAAACCCCGTCATC-3'. These primers generate a 1.1-kbp fragment from MR₁ genomic DNA and a 1.6-kbp fragment if uvsE is replaced by the deletion cassette. The recombinant from which only the 1.6-kbp version was produced was designated TNK001. TNK003 was constructed in the same manner as TNK001 was constructed from strain 302: uvrA1 was mutagenized by N-methyl-N'-nitro-N-nitrosoguanidine treatment (9).

To generate strain TNK002, a 2.8-kbp SalI-SmaI fragment of genomic DNA corresponding to the downstream region of uvrA2 was inserted upstream of a hygromycin resistance cassette in pKatHPH3, a hygromycin-resistant version of pKatCAT (4). The resulting plasmid was ligated with a 3.2-kbp EagI-HindIII fragment, upstream of uvrA2, generating pTNK007 in which a hygromycin resistance cassette is fused downstream and upstream of uvrA2. D. radiodurans MR₁ cells were transformed with the hybrid fragment and spread on TGY plates containing 37.5 µg/ml hygromycin. Recombinants were screened for a disrupted uvrA2 using primers 5'-TTCGGTTGTGGTCACATCGTC-3' and 5'-CGTGTTCCACCACGAACAGG-3'. These primers amplify a 1.6-kbp fragment from the MR₁ genome, and a 1.8-kbp fragment is generated when uvrA2 is replaced with the disruption cassette. Amplification of genomic DNA from strain TNK002 produced the 1.8-kbp version. Strains TNK004, TNK005, and TNK006 were constructed by inactivating uvrA2 in strains TNK001, 302, and TNK003, respectively.

Strain TNK007 was generated as described previously (12). Briefly, a recA229::cat fragment of pKSCR3 was used to transform strain MR₁, and genomic DNA of a recombinant selected on TGY plates containing 3 µg/ml chloramphenicol was screened by PCR using 5'-AACGCAGCAAGGCCATCGAAAC-3' and 5'-ACCAGCAGTTCGTCGGTGTTCA-3'. These primers amplify a 0.3-kbp fragment from MR₁ genomic DNA or a 1.2-kbp fragment corresponding to the disruption cassette when recA is disrupted.

Enzyme-linked immunosorbent assays (ELISAs) for CPDs and 6-4PPs. ELISAs were performed to determine the repair kinetics of CPDs and 6-4PPs as described previously (7, 8). Briefly, cells irradiated with 600 J/m² of UV were resuspended in TGY and incubated at 30°C with shaking. Aliquots were harvested at various time points for the preparation of DNA. The amount of CPDs or 6-4PPs in genomic DNA from each aliquot was measured by an ELISA. To detect CPDs, 6 ng of DNA was reacted with TDM-2 antibodies. For the detection of 6-4PP with 64M-2 antibodies, 30 ng of DNA was used.

Top Abstract Introduction Materials and Methods Results Discussion References

 
To determine the relative contributions of UVER and NER and the role of UvrA2 in UV resistance, we examined the sensitivity to UV of mutants lacking uvsE, uvrA1, and/or uvrA2. In our conditions, cells with a single mutation of uvsE or uvrA1 showed changes in sensitivity. The uvrA1 strain displayed slightly higher sensitivity than the wild type, while an extremely high dose of radiation was lethal in the uvsE mutant (Fig. 1). These observations are consistent with the notion that in S. pombe, NER is more relevant to UV resistance than UVER (16, 17), although a previous study reported that the loss of uvrA1 or uvsE alone had no effect on survival in D. radiodurans (2). This may reflect the difference in the capacity to recover from UV damage between rapidly growing cells and early stationary-phase cells in Deinococcus. It has been reported that the contributions of NER and UVER pathways to UV resistance in S. pombe depend on the growth phase (16). Our data suggest that the roles of deinococcal UVER and NER in the recovery from UV damage are increased in stationary-phase cells than in exponential-phase cells. Figure 1 also indicates that the loss of uvrA2 had no deleterious effect on survival of wild-type, uvrA1 mutant, and uvsE mutant cells.

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FIG. 1. UV survival curves for D. radiodurans strain MR1 and mutants lacking uvsE, uvrA1, and/or uvrA2. Each point represents the average ± standard deviation (error bar) of at least three independent experiments. WT, wild type.

When uvsE was disrupted in the uvrA1 background, the resulting strain displayed synergistically decreased UV resistance (Fig. 2), showing the overlap in the functions of the UVER and NER pathways to recover from UV damage as previously reported (2). In addition, we have found that inactivation of the uvrA2 gene in the uvsE uvrA1 background had no effect on survival (Fig. 2), suggesting a minor role for UvrA2 in the resistance to UV. Furthermore, loss of uvsE, uvrA1, and uvrA2 was found to cause no increase in UV-induced mutations (Fig. 3), implying that UVER, NER, and UvrA2 do not significantly contribute to the resistance to the mutagenic effect of UV in this species. In terms of UV resistance pathways other than excision repair mechanisms, HR could be critical in this species, because a deinococcal recA strain was extremely sensitive to UV (5). We have found that the recA single mutant showed greater sensitivity to UV than the uvsE uvrA1 and uvsE uvrA1 uvrA2 mutants (Fig. 2). Therefore, it is suggested that the function of RecA is more significant than that of two different excision repair pathways for UV resistance in this species and that the recovery from UV damage of the uvsE uvrA1 and uvsE uvrA1 uvrA2 strains depends on the remaining mechanisms of resistance, including HR.

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FIG. 2. UV survival curves for three mutant D. radiodurans strains (uvsE uvrA1, uvsE uvrA1 uvrA2, and recA mutants). Values are means ± standard deviations (error bars).

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FIG. 3. Mutation frequencies for D. radiodurans strain MR1 and uvsE uvrA1 and uvsE uvrA1 uvrA2 mutant strains with (+) or without (–) exposure to UV. Values are means ± standard deviations (error bars). WT, wild type.

To determine the capacities of deinococcal UVER and NER pathways to remove CPDs and 6-4PPs, we measured the repair rate for each photoproduct by an ELISA (Fig. 4). We have found that both CPDs and 6-4PPs were removed in uvsE, uvrA1, and uvsE uvrA1 mutants, although the kinetics of the respective repair process was influenced by the pathway inactivated. When uvrA1 was lost in addition to uvsE, the repair of 6-4PPs was less efficient than that in the uvsE mutant, whereas the rates of removal of CPDs in the uvsE strain and uvsE uvrA1 strain were comparable. This result indicates that the NER pathway of D. radiodurans removes 6-4PPs from UV-irradiated DNA but plays a minor role in the removal of CPDs. In contrast, loss of uvsE in the uvrA1 background reduced the repair rates of CPDs and 6-4PPs relative to those of the uvrA1 mutant, revealing that UVER removes both lesions. On the other hand, loss of uvrA2 did not remarkably affect the repair kinetics in the uvsE uvrA1 strain (Fig. 4) or those in the wild-type, uvsE, and uvrA1 strains (data not shown), indicating a minor role for UvrA2 in the repair of CPDs and 6-4PPs.

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FIG. 4. Removal of CPDs and 6-4PPs from genomic DNA in UV-irradiated D. radiodurans strain MR1 and uvsE, uvrA1, uvsE uvrA1, and uvsE uvrA1 uvrA2 mutant strains. Each point represents the average ± standard deviation (error bar) of at least three independent experiments. WT, wild type.

Top Abstract Introduction Materials and Methods Results Discussion References

 
Our epistatic analysis supports the hypothesis that the UVER and NER pathways function independently to counteract the deadly effects of UV in D. radiodurans (2). We also determined the relative contributions of UVER, NER, and the RecA-dependent process to the resistance to UV in D. radiodurans. In addition, we biochemically demonstrated the properties of UVER and NER of CPDs and 6-4PPs. However, the biological significance of UvrA2 to UV resistance remains unclear. Our data indicate a minor role for UvrA2 in the resistance to UV-induced killing and mutagenesis and in the removal of CPDs and 6-4PPs. This may suggest yet another function of UvrA2 protein in cellular metabolism.

Since the deinococcal UVER pathway efficiently eliminates both CPDs and 6-4PPs, this pathway is an important component of the UV damage repair system, as in S. pombe (17). In contrast, the deinococcal NER pathway does not significantly contribute to the removal of CPDs, though it efficiently repairs 6-4PPs, suggesting a critical role for the repair pathways in dealing with 6-4PPs. It is also suggested that loss of NER results in biological consequences of UV mainly caused by 6-4PPs. Here we argue that 6-4PPs are mainly responsible for the killing of cells in Deinococcus. When both UVER and NER were inactivated, the resulting strain showed a synergistic increase in sensitivity to UV relative to each single mutant. On the other hand, the numbers of CPDs remaining in the UVER-defective strain and UVER plus NER-defective strain were comparable, although the rate of repair of 6-4PPs was reduced in the strain lacking both UVER and NER. Therefore, it is possible that the relative roles of CPDs and 6-4PPs are different in this species; 6-4PPs have a more lethal effect on D. radiodurans than do CPDs. In this respect, the response of D. radiodurans to UV is similar to that of NER-deficient human cells in which 6-4PPs are more toxic than CPDs (10).

On the basis of photoreactivation studies, it has been reported that cytosine-containing pyrimidine dimers are most responsible for UV-induced mutagenesis (13, 14). Since 67% of the genome is composed of cytosine and guanine base pairs (15), the deinococcal genomic DNA should be susceptible to UV mutagenesis. However, the frequency of mutation was not increased by UV in spite of the loss of UVER, NER, and UvrA2 in our Rif assay. This suggests that D. radiodurans does not possess DNA polymerases for TLS or that the TLS is remarkably error free. Alternatively, it is possible that this bacterium possesses mechanisms to remove UV photoproducts in addition to UVER and NER. Actually, our data showed that both CPDs and 6-4PPs were eliminated even in the absence of UVER and NER (Fig. 4). We have also found that the recA mutant was more sensitive to UV than the strain lacking both UVER and NER (Fig. 2). Since the deinococcal RecA forms a filament on the double-stranded DNA (6), the damaged strand would be processed by HR in this species. Therefore, HR would help to remove UV photoproducts from genomic DNA in this species. In this context, the major role of RecA in resistance to UV in D. radiodurans seems to be different from that in E. coli. HR in E. coli does not significantly contribute to the elimination of CPDs in the uvrA background, whereas RecA plays an indirect role in the repair of damage by amplifying UvrA in the SOS response to fully accomplish NER (7). This also suggests a difference in the gene regulatory mechanism for UV resistance in the two organisms. In Deinococcus, recA expression is stimulated by IrrE, a regulator unique to this bacterium, after exposure to ionizing radiation, and the loss of irrE reduces the resistance to UV as well as ionizing radiation (1). This implies a significant role for the IrrE-associated regulatory system in resistance to UV as well. Investigations of the transcriptional response to UV may identify novel components responsible for resistance and provide insights into the mechanisms that regulate the expression of excision repair genes and HR genes, leading to a better understanding of exactly how this species copes with exposure to UV.

 
This work was supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology, Japan. M.T. is the recipient of a scholarship from the Japan Atomic Energy Research Institute.

 
* Corresponding author. Mailing address: Department of Biomolecular Sciences, Graduate School of Life Sciences, Tohoku University, Sendai 980-8577, Japan. Phone: (81)-22-217-5054. Fax: (81)-22-217-5053. E-mail: yamamot{at}mail.tains.tohoku.ac.jp.

Present address: Department of Immunology, Graduate School of Medical and Dental Sciences, Kagoshima University, Kagoshima 890-8544, Japan.

Top Abstract Introduction Materials and Methods Results Discussion References

 

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Journal of Bacteriology, June 2005, p. 3693-3697, Vol. 187, No. 11
0021-9193/05/$08.00+0     doi:10.1128/JB.187.11.3693-3697.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

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