Interplay between replication and recombination in Escherichia coli: Impact of the alternative DNA polymerases
- Institut National de la Santé et de la Recherche Médicale U571, Faculté de Médecine “Necker-Enfants Malades” Université Paris V, 156 Rue de Vaugirard, 75730 Paris Cedex 15, France
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Edited by Philip C. Hanawalt, Stanford University, Stanford, CA, and approved January 23, 2006 (received for review October 14, 2005)
Abstract
Homologous recombination (HR) and translesion synthesis (TLS) are two pathways involved in the tolerance of lesions that block the replicative DNA polymerase. However, whereas TLS is frequently error-prone and, therefore, can be deleterious, HR is generally error-free. Furthermore, because the recombination enzymes and alternative DNA polymerases that perform TLS may use the same substrate, their coordination might be important to assure cell fitness and survival. This study aimed to determine whether and how these pathways are coordinated in Escherichia coli cells by using conjugational replication and recombination as a model system. The role of the three alternative DNA polymerases that are regulated by the SOS system was tested in DNA polymerase III holoenzyme-proficient and -deficient mutants. When PolIII is inactive, the alternative DNA polymerases copy DNA in the following order: PolII, PolIV, and PolV. The observed hierarchy corresponds to the selective constraints imposed on the genes coding for alternative DNA polymerases observed in natural populations of E. coli, suggesting that this hierarchy depends on the frequency of specific damages encountered during the evolutionary history of E. coli. We also found that DNA replication and HR are in competition and that they can precede each other. Our results suggest that there is probably not an active choice of which pathway to use, but, rather, the nature and concentration of lesions that lead to formation of ssDNA and the level of SOS induction that they engender might determine the outcome of the competition between HR and alternative DNA polymerases.
Footnotes
- †To whom correspondence should be addressed. E-mail: matic{at}necker.fr
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Author contributions: S.D. and I.M. designed research; S.D. performed research; S.D. contributed new reagents/analytic tools; S.D. and I.M. analyzed data; and S.D. and I.M. wrote the paper.
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Conflict of interest statement: No conflicts declared.
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This paper was submitted directly (Track II) to the PNAS office.
- Abbreviations:
- HR,
- homologous recombination;
- PolIII,
- DNA polymerase III holoenzyme;
- TLS,
- translesion synthesis.
- © 2006 by The National Academy of Sciences of the USA
