DNA toroids: framework for DNA repair in Deinococcus radiodurans and in germinating bacterial spores.

Abstract

Bacteria belonging to the family Deinococcaceae survive exposure to >1.5 megarads of ionizing irradiation or to extreme desiccation without lethality or mutagenesis (2, 31, 35). This tolerance derives from the ability of these species to accurately mend numerous double-strand DNA breaks (DSBs), thus reassembling an intact genome from hundreds of fragments in a manner that restores chromosomal continuity. The only known mechanism that enables accurate repair of DSBs in bacteria is RecA-dependent homologous recombination, whereby information lost at a lesion is restored by a homologous DNA sequence that acts as a template (22-24). As such, DNA repair via homologous recombination strictly depends upon the ability of cellular systems to perform a rapid and efficient genomewide search for homologous DNA sites (27). However, following extensive DNA fragmentation, no intact template remains. Homologous search conducted under such circumstances would necessarily entail repetitive reinspection of multiple randomly dispersed DNA fragments, rendering the process inherently futile (9a, 36). Indeed, the first phase of DNA repair in Deinococcus radiodurans was shown to be RecA independent (9), implying that this phase does not rely on homologous recombination. The high resistance of bacterial spores to irradiation and desiccation indicates that DSBs inflicted by these assaults on dormant spores are efficiently and accurately mended upon germination. However, DNA repair involving homologous search processes cannot occur in germinating spores, because bacterial spores regularly carry only one copy of their genomes (5). Consequently, germinating spores lack the template required for accurate homologous-recombination-mediated repair of DSBs.