<em>Deinococcus geothermalis</em>: The Pool of Extreme Radiation Resistance Genes Shrinks

Abstract

<div><p>Bacteria of the genus <em>Deinococcus</em> are extremely resistant to ionizing radiation (IR), ultraviolet light (UV) and desiccation. The mesophile <em>Deinococcus radiodurans</em> was the first member of this group whose genome was completely sequenced. Analysis of the genome sequence of <em>D. radiodurans</em>, however, failed to identify unique DNA repair systems. To further delineate the genes underlying the resistance phenotypes, we report the whole-genome sequence of a second <em>Deinococcus</em> species, the thermophile <em>Deinococcus geothermalis</em>, which at its optimal growth temperature is as resistant to IR, UV and desiccation as <em>D. radiodurans</em>, and a comparative analysis of the two <em>Deinococcus</em> genomes. Many <em>D. radiodurans</em> genes previously implicated in resistance, but for which no sensitive phenotype was observed upon disruption, are absent in <em>D. geothermalis</em>. In contrast, most <em>D. radiodurans</em> genes whose mutants displayed a radiation-sensitive phenotype in <em>D. radiodurans</em> are conserved in <em>D. geothermalis</em>. Supporting the existence of a <em>Deinococcus</em> radiation response regulon, a common palindromic DNA motif was identified in a conserved set of genes associated with resistance, and a dedicated transcriptional regulator was predicted. We present the case that these two species evolved essentially the same diverse set of gene families, and that the extreme stress-resistance phenotypes of the <em>Deinococcus</em> lineage emerged progressively by amassing cell-cleaning systems from different sources, but not by acquisition of novel DNA repair systems. Our reconstruction of the genomic evolution of the <em>Deinococcus-Thermus</em> phylum indicates that the corresponding set of enzymes proliferated mainly in the common ancestor of <em>Deinococcus</em>. Results of the comparative analysis weaken the arguments for a role of higher-order chromosome alignment structures in resistance; more clearly define and substantially revise downward the number of uncharacterized genes that might participate in DNA repair and contribute to resistance; and strengthen the case for a role in survival of systems involved in manganese and iron homeostasis.</p></div>