Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks

Journal Article · Mon Jan 01 04:00:00 EST 2007 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0000955· OSTI ID:936820

Makarova, Kira S ^[1]; Omelchenko, Marina ^[1]; Gaidamakova, Elena ^[2]; Matrosova, Vera ^[2]; Vasilenko, Alexander ^[2]; Zhai, Min ^[2]; Lapidus, Alla L ^[3]; Copeland, A ^[3]; Kim, Edwin ^[3]; Land, Miriam L ^[4]; Mavromatis, K ^[3]; Pitluck, Samual ^[3]; Richardson, P M ^[3]; Detter, J Chris ^[3]; Brettin, Tom ^[5]; Saunders, Elizabeth H ^[5]; Lai, Barry ^[6]; Ravel, Bruce ^[6]; Kemner, Kenneth M ^[6]; Wolf, Yuri ^[1] ; Sorokin, Alexei ^[7]; Gerasimova, Anna ^[8]; Gelfand, Mikhail ^[9]; Fredrickson, James K ^[10]; Koonin, Eugene ^[1]; Daly, Michael ^[2]

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1. National Center for Biotechnology Information
2. Uniformed Services University of the Health Sciences (USUHS)
3. U.S. Department of Energy, Joint Genome Institute
4. ORNL
5. Los Alamos National Laboratory (LANL)
6. Argonne National Laboratory (ANL)
7. Genetique Microbienne
8. Research Institute of Genetics and Selection of Industrial Microorganisms, Mosco
9. Moscow State University
10. Pacific Northwest National Laboratory (PNNL)

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.

• Research Organization: Oak Ridge National Laboratory (ORNL)
• Sponsoring Organization: SC USDOE - Office of Science (SC)
• DOE Contract Number: AC05-00OR22725
• OSTI ID: 936820
• Journal Information: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 9 Vol. 2
• Country of Publication: United States
• Language: English

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
ALIGNMENT
BACTERIA
CHROMOSOMES
DNA
DNA REPAIR
ENZYMES
GENES
HOMEOSTASIS
IONIZING RADIATIONS
IRON
MANGANESE
MUTANTS
PHENOTYPE
RADIATIONS