Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks

National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, Maryland, USA.
PLoS ONE (Impact Factor: 3.23). 02/2007; 2(9):e955. DOI: 10.1371/journal.pone.0000955
Source: PubMed


Bacteria of the genus Deinococcus are extremely resistant to ionizing radiation (IR), ultraviolet light (UV) and desiccation. The mesophile Deinococcus radiodurans was the first member of this group whose genome was completely sequenced. Analysis of the genome sequence of D. radiodurans, 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 Deinococcus species, the thermophile Deinococcus geothermalis, which at its optimal growth temperature is as resistant to IR, UV and desiccation as D. radiodurans, and a comparative analysis of the two Deinococcus genomes. Many D. radiodurans genes previously implicated in resistance, but for which no sensitive phenotype was observed upon disruption, are absent in D. geothermalis. In contrast, most D. radiodurans genes whose mutants displayed a radiation-sensitive phenotype in D. radiodurans are conserved in D. geothermalis. Supporting the existence of a Deinococcus 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 Deinococcus 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 Deinococcus-Thermus phylum indicates that the corresponding set of enzymes proliferated mainly in the common ancestor of Deinococcus. 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.

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    • "One such hypothesis regards the manganese content and manganese to iron ratio observed in radiation tolerant bacteria [16]. There are similar distributions of manganese and iron in different radiation tolerant bacteria [17] but different distributions compared to radiation sensitive bacteria [18]. Although such correlative patterns do not necessarily imply a causal relationship between manganese and radiation tolerance, they do provide a hypothesis that may be evaluated by techniques identifying specific elements and their distribution in the body. "
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    • "N o n c o m m e r c i a l u s e o n l y that prevent or inactivate the damaging reactive oxygen species (ROS) that arise when radiation hits the water molecules, and that manganese performs such a role to protect the cell from ROS after irradiation. Later studies showed that also another radiation tolerant bacterium (Deinoccocus geothermalis) has high manganese/iron (Mn/Fe) accumulation (Daly et al., 2007), and that not only the levels but also the distributions of Mn and Fe in these two bacteria are essentially the same (Makarova et al., 2007). In these analyses, and also in a study of elemental composition of the gram-negative bacterium Pseudomonas fluorescens (Flügge) Migula, 1895 (Kemner et al., 2004), elements were determined using X-ray fluorescence analysis (XRF). "
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    • "A 17-bp palindromic motif was found upstream of 11 genes: gyrA, gyrB, ssb, pprA, ddrB, ddrD, uvrD, recAC, recAP1, recAP3 and Deide_02842 (Type II restriction enzyme). This motif corresponds to the radiation/desiccation response motif (RDRM) first identified after analysis of radiation-induced genes in D. radiodurans and D. geothermalis[36]. In a previous study we scanned the entire genome of D. deserti with this motif and a match with the RDRM was found in the upstream region of 25 genes, including 10 of the 11 genes mentioned above [4]. "
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