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Title: Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks

Abstract

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 lineagemore » 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.« less

Authors:
 [1];  [1];  [2];  [2];  [2];  [2];  [3];  [3];  [3];  [4];  [3];  [3];  [3];  [3];  [5];  [5];  [6];  [6];  [6];  [1] more »;  [7];  [8];  [9];  [10];  [1];  [2] « less
  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)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
936820
DOE Contract Number:  
DE-AC05-00OR22725
Resource Type:
Journal Article
Resource Relation:
Journal Name: PLoS ONE; Journal Volume: 2; Journal Issue: 9
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; ALIGNMENT; BACTERIA; CHROMOSOMES; DNA; DNA REPAIR; ENZYMES; GENES; HOMEOSTASIS; IONIZING RADIATIONS; IRON; MANGANESE; MUTANTS; PHENOTYPE; RADIATIONS

Citation Formats

Makarova, Kira S., Omelchenko, Marina, Gaidamakova, Elena, Matrosova, Vera, Vasilenko, Alexander, Zhai, Min, Lapidus, Alla L., Copeland, A, Kim, Edwin, Land, Miriam L, Mavromatis, K, Pitluck, Samual, Richardson, P M, Detter, J. Chris, Brettin, Tom, Saunders, Elizabeth H, Lai, Barry, Ravel, Bruce, Kemner, Kenneth M, Wolf, Yuri, Sorokin, Alexei, Gerasimova, Anna, Gelfand, Mikhail, Fredrickson, James K, Koonin, Eugene, and Daly, Michael. Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks. United States: N. p., 2007. Web. doi:10.1371/journal.pone.0000955.
Makarova, Kira S., Omelchenko, Marina, Gaidamakova, Elena, Matrosova, Vera, Vasilenko, Alexander, Zhai, Min, Lapidus, Alla L., Copeland, A, Kim, Edwin, Land, Miriam L, Mavromatis, K, Pitluck, Samual, Richardson, P M, Detter, J. Chris, Brettin, Tom, Saunders, Elizabeth H, Lai, Barry, Ravel, Bruce, Kemner, Kenneth M, Wolf, Yuri, Sorokin, Alexei, Gerasimova, Anna, Gelfand, Mikhail, Fredrickson, James K, Koonin, Eugene, & Daly, Michael. Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks. United States. doi:10.1371/journal.pone.0000955.
Makarova, Kira S., Omelchenko, Marina, Gaidamakova, Elena, Matrosova, Vera, Vasilenko, Alexander, Zhai, Min, Lapidus, Alla L., Copeland, A, Kim, Edwin, Land, Miriam L, Mavromatis, K, Pitluck, Samual, Richardson, P M, Detter, J. Chris, Brettin, Tom, Saunders, Elizabeth H, Lai, Barry, Ravel, Bruce, Kemner, Kenneth M, Wolf, Yuri, Sorokin, Alexei, Gerasimova, Anna, Gelfand, Mikhail, Fredrickson, James K, Koonin, Eugene, and Daly, Michael. Mon . "Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks". United States. doi:10.1371/journal.pone.0000955.
@article{osti_936820,
title = {Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks},
author = {Makarova, Kira S. and Omelchenko, Marina and Gaidamakova, Elena and Matrosova, Vera and Vasilenko, Alexander and Zhai, Min and Lapidus, Alla L. and Copeland, A and Kim, Edwin and Land, Miriam L and Mavromatis, K and Pitluck, Samual and Richardson, P M and Detter, J. Chris and Brettin, Tom and Saunders, Elizabeth H and Lai, Barry and Ravel, Bruce and Kemner, Kenneth M and Wolf, Yuri and Sorokin, Alexei and Gerasimova, Anna and Gelfand, Mikhail and Fredrickson, James K and Koonin, Eugene and Daly, Michael},
abstractNote = {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.},
doi = {10.1371/journal.pone.0000955},
journal = {PLoS ONE},
number = 9,
volume = 2,
place = {United States},
year = {Mon Jan 01 00:00:00 EST 2007},
month = {Mon Jan 01 00:00:00 EST 2007}
}