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Journal of Bacteriology, November 2006, p. 7977-7980, Vol. 188, No. 22
0021-9193/06/$08.00+0     doi:10.1128/JB.01088-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Role of DNA Polymerase IV in Escherichia coli SOS Mutator Activity{triangledown}

Wojciech Kuban,1 Magdalena Banach-Orlowska,1 Roel M. Schaaper,2 Piotr Jonczyk,1 and Iwona J. Fijalkowska1*

Institute of Biochemistry and Biophysics, Polish Academy of Sciences, 02 106 Warsaw, Poland,1 Laboratory of Molecular Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 277092

Received 22 July 2006/ Accepted 8 September 2006


   ABSTRACT
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Constitutive expression of the SOS regulon in Escherichia coli recA730 strains leads to a mutator phenotype (SOS mutator) that is dependent on DNA polymerase V (umuDC gene product). Here we show that a significant fraction of this effect also requires DNA polymerase IV (dinB gene product).


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In Escherichia coli two members of the Y family of polymerases are expressed as part of the inducible SOS response—DNA polymerase IV (Pol IV) and DNA Pol V. Both lack intrinsic proofreading activity and are considered low-fidelity DNA polymerases (14, 32, 33). Pol IV is encoded by the dinB gene (10, 24, 36). In normal cells, Pol IV is present at a relatively high level (~250 molecules per cell) (13), compared to an estimated 30 molecules of the replicative Pol III (19). Upon SOS induction the Pol IV levels are increased by an additional 10-fold (13). The precise role of Pol IV under both normal and SOS-induced conditions is still under active investigation. In normal cells, the presence of Pol IV was shown to enhance the long-term survival and evolutionary fitness of E. coli (46). It has further been proposed that the major function of Pol IV is the restart of stalled replication forks (8). With regard to mutagenesis, a number of studies have indicated that Pol IV does not significantly affect the level of spontaneous mutations on the bacterial chromosome in growing cells (16, 21, 43), suggesting that it has limited access to the normal chromosomal growing point. On the other hand, Pol IV plays some role in mutagenesis on F' episomes (16) and contributes significantly to mutagenesis occurring in resting cells (adaptive mutagenesis) (6, 20, 35). Pol IV is able to carry out error-free or error-prone translesion synthesis, depending upon the nature of DNA damage and the sequence context (23), and has been shown to be involved in mutagenesis induced by 4-nitroquinoline-N-oxide, B[a]P-guanine adducts, and oxidative damage (9, 13, 17, 23, 30, 38).

DNA Pol V is a heterotrimeric complex (UmuD'2C) containing the umuC gene product, representing the catalytic subunit, and two copies of UmuD', a RecA-produced proteolytic fragment of UmuD (28, 33). Pol V is required for most or all of SOS mutagenesis. Its intracellular concentration in normal cells is below the level of detection (<15 molecules per cell) (44). Upon full induction the umuDC operon produces approximately 2,400 molecules of UmuD and 200 molecules of UmuC. How many molecules of active Pol V are present under such conditions is an open question, as its components are tightly regulated both transcriptionally and posttranscriptionally (see reference 45 for a review). Pol V is proficient in bypassing UV-induced pyrimidine dimers and abasic sites in vitro (28, 32, 33), and this proficiency underlies its critical role in damage-induced mutagenesis in vivo.

One interesting and experimentally informative aspect of the SOS response is the SOS mutator activity. This mutator activity is observed in strains that carry a constitutively activated RecA protein (e.g., RecA441 or RecA730) (34, 40, 41). Activation of RecA is an initiating event in SOS induction when replication is blocked by DNA damage; however, in constitutively activated recA mutants, the SOS system is constitutive in the absence of any overt DNA damage. Like DNA damage-induced SOS mutagenesis, this SOS mutator activity depends on the action of Pol V (3, 31, 42). Studies of the SOS mutator phenotype in recA730-carrying strains have indicated that the mutator effect reflects a Pol V-dependent increase in the production of DNA replication errors rather than error-prone events at endogenous DNA lesions (2, 4). Mechanistically, Pol V was proposed to interfere with ongoing chromosomal replication through the error-prone extension of terminal mismatches created by Pol III holoenzyme (HE) (the enzyme that performs replication of the E. coli chromosome), which may temporarily stall at such mismatches (4, 25, 26).

A question that has not received much attention is the possible role of Pol IV in the SOS mutator activity. Pol IV is strongly induced under these conditions, and a possible role for this enzyme should be considered. When Pol IV is overproduced in otherwise normal, uninduced strains, a mutator effect is observed (12, 15, 37), indicating the mutagenic potential of this enzyme. Here, we have addressed this question by investigating the SOS mutator activity in recA730 strains in the presence and absence of Pol IV.

The experimental system that we used to assess mutant frequencies has as an additional feature that it can provide information about mutagenesis that might specifically result from either leading- or lagging-strand replication. In the system, which has been described in detail elsewhere (5, 7, 18), we compare the mutability of defined lacZ markers in pairs of strains containing the lac operon in two orientations relative to the direction of replication. Within any given pair, a lac sequence of interest is replicated by the lagging-strand machinery in one strain and by the leading-strand machinery in the other, and any difference in mutability of the target gene between the two orientations is most readily interpreted in terms of a difference in fidelity of leading- and lagging-strand DNA synthesis. Previous results with this system have revealed that in normal cells lagging-strand replication is most accurate but that in recA730 strains, as well as in Pol IV-overproducing cells, lagging-strand errors are preferentially enhanced (1, 5, 16, 18).

Wild-type, recA730, mutL, and recA730 mutL strains containing two lac alleles (for measurement of either G · C->T · A or A · T->T · A transversions) in the two chromosomal orientations have been described elsewhere (5, 18). Mismatch-repair-defective mutL derivatives are often useful in these studies to facilitate interpretation of the results in terms of (uncorrected) replication errors. The two lac alleles chosen respond readily to SOS induction by the recA730 allele (4, 18). The strains were made defective in Pol IV activity by introducing the {Delta}dinB::kan deletion (12, 13) by P1 transduction. The results for these experiments are shown in Table 1. The data for the recA730 (dinB+) strains reproduce the previously published results (18). For both lac alleles, recA730 increases mutagenesis significantly, with the largest increase occurring for the lac orientation (R) for which mutagenesis reflects events on the lagging strand (5, 18). For example, for the G · C->T · A transversions, the recA730 effects are 15-fold (5.9/0.4) (R) and 5-fold (3.5/0.7) (L) in the mutL+ background and 28-fold (37/1.3) (R) and 2-fold (3.6/1.7) (L) in the mutL background. For the A · T->T · A transversions, we observe 150-fold (45/0.3) (R) and 5-fold (3.7/0.7) (L) effects in the mutL+ background and 48-fold (48/1.0) (R) and 10-fold (11/1.1) (L) effects for the mutL strain.


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  		TABLE 1. Effect of dinB deletion on lac reversion frequencies in normal and SOS-induced (recA730) cells

 
Importantly, Table 1 also shows that the loss of Pol IV ({Delta}dinB::kan) significantly reduces the mutator activity of the recA730 strains. For the G · C->T · A transversions, there was a greater-than-threefold decrease of mutability in the R orientation (corresponding to the lagging strand) in either mutL+ or mutL backgrounds. For the A · T->T · A transversions, greater than half (2.8- and 2.2-fold, respectively) of the recA730-dependent mutations in this orientation were dinB dependent. In the mutL background, a 2.4-fold decrease was also observed for the L orientation. It appears that as much as 70% of the mutations in recA730 strains may require the action of Pol IV, and we therefore conclude that Pol IV is a significant contributor to the recA730-mediated mutator effect. Secondly, this contribution of Pol IV is strongest on the lagging strand. Finally, as expected (3, 31, 41), lack of Pol V ({Delta}umuDC::cat) abolishes mutagenesis nearly completely to the level of the wild-type strain (Table 1, last group). The results indicate that both Pol IV and Pol V have significant access to the replication fork under SOS-induced conditions. However, their functions are likely to be different, as lack of Pol V abolishes nearly all SOS mutator effect, while lack of Pol IV may abolish 50 to 70%.

Overproduction of Pol IV from a multicopy dinB plasmid, in otherwise normal cells, results in a mutator phenotype (12, 15, 37). This effect is independent of recA or umuDC (37) and therefore does not involve Pol V. We previously showed that this Pol IV mutator effect has preference for the lagging strand (15). In view of the role of Pol IV in the SOS mutator effect as demonstrated above, we undertook to investigate the effect of Pol IV overproduction in recA730 strains. We measured the lac G · C->T · A transversion, as this event is particularly susceptible to Pol IV overproduction, even from a low-copy-number plasmid (15). The data in Table 2 indicate that the low-copy-number dinB plasmid pLO1 (15) significantly enhanced the frequency of mutations in each of the indicated backgrounds, including recA730. In the recA730 strains, the dinB plasmid enhanced the SOS mutator effect by 2.7- and 6.6-fold for leading and lagging strands, respectively. These effects are significantly larger than would be expected based on simple additivity of the two separate mutator effects. We therefore conclude that Pol IV and Pol V likely cooperate in producing the mutations.


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  		TABLE 2. Lac reversion frequency (number of revertants per 108 cells) in strains carrying low-copy-number dinB plasmid pLO1a

 
We have previously proposed that the SOS mutator effect reflects most plausibly the error-prone extension—by Pol V—of terminal mismatches created as replication errors made by Pol III HE (18). HE has significant difficulty continuing DNA synthesis from mismatches (11, 22, 25, 26), and the stalling that ensues at such a mismatch is a likely step-up point for other DNA polymerases, such as Pol V, if present. Alternatively, the mutator effect may result from the high intrinsic error rate of Pol V. This possibility cannot be excluded, although calculations (15, 18) suggested that this would require very significant amounts of DNA synthesis by this enzyme (1 to 10% of the chromosome). Similarly, extension of Pol III misinsertion errors by Pol IV was proposed to underlie the Pol IV mutator effect (15). Both effects—SOS and Pol IV mutator—were greatest in the lagging strand, presumably reflecting the fact that the dissociative tendencies of Pol III are greatest in this strand. In both cases, transversion mutations are preferentially enhanced, further consistent with transversion mismatches (either Pyr · Pyr or Pur · Pur) being the most difficult to extend for Pol III (11). Despite these similarities, the two mutator effects differ in their specificity (15, 18), likely reflecting the differential ability of Pol IV and V to process specific terminal mismatches and/or to create specific polymerization errors.

In view of the above models, the role of Pol IV in the SOS mutator activity may be explained through a sequential, multistep pathway. In a first possible scenario, an initial error is made by Pol III HE. The resulting mismatch may lead to dissociation of Pol III, either spontaneously or in a directed fashion, perhaps by action of the Pol III {tau} subunit as proposed previously (27). Formation of the RecA filament at the site of Pol III dissociation will then permit preferential access of Pol V (29), accounting for the near-complete dependence of the mutator effect on this enzyme. Nevertheless, synthesis by Pol V may not be processive enough and/or the RecA filament may not be long-lived enough to fix the mutation. In those instances, the role of Pol IV may be to further extend the primer protecting it against the action of the exonuclease action of the proofreading-proficient enzymes and ultimately fixing the mutation. In a more extreme version of this model, Pol V, after having displaced Pol III from the mismatched primer, may itself fail to extend the mismatch in a fraction of the cases, and Pol IV may then be required for the extension step. In a different scenario, Pol V may gain access to the replication fork in the absence of Pol III-mediated error. Pol V may then produce occasional insertion errors, which may require fixing, at least part of the time, by the action of Pol IV. While both Pol V and Pol IV are generally inaccurate enzymes, their fidelity properties at both the misinsertion and mismatch extension steps are different and, in part, complementary. We have also considered models involving more than one error, for example, one error by Pol III, facilitating transfer to Pol V, and a subsequent one by Pol V, facilitating transfer to Pol IV, but the DNA sequencing of 30 lac revertants in a recA730 strain (involving, in each mutant, some 550 nucleotides around the lac reversion site) failed to reveal any second mutation.

Overall, the current results add to the increasing body of information regarding the role(s) of Pol IV in E. coli.


   ACKNOWLEDGMENTS
 
We thank Miguel Garcia-Diaz and Gary Schultz of the NIEHS for their helpful comments on the manuscript.

This research was supported by grant 2 PO4A 023 029 from the Polish Ministry of Scientific Research and Information Technology, State Committee for Scientific Research, and by the Intramural Research Program of the NIH, National Institute of Environmental Health Sciences.


   FOOTNOTES
 
* Corresponding author. Mailing address: Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawinskiego 5A 02 106 Warsaw, Poland. Phone: (48) 22-592-1113. Fax: (48) 22-658-4636. E-mail: iwonaf{at}ibb.waw.pl. Back

{triangledown} Published ahead of print on 15 September 2006. Back


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Journal of Bacteriology, November 2006, p. 7977-7980, Vol. 188, No. 22
0021-9193/06/$08.00+0     doi:10.1128/JB.01088-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.




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