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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}
}
  • 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 itsoptimal growth temperature is as resistant to IR, UV and desiccation as D. radiodurans, and a comparative analysis of the two Deinococcus genomes. Many D. radioduransmore » 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.« less
  • The whole-genome sequence of Deinococcus geothermalis is the second for an extremely ionizing radiation (IR) resistant bacterium. The first was for Deinococcus radiodurans, which for 50 years has been the subject of extensive investigations aimed at solving the mystery of how this microbe can survive immense doses of x-rays. So far, comparative analyses between the genome of D. radiodurans and genomes of other bacteria have failed to produce a coherent picture of the underlying resistance systems. Most surprisingly, many critical DNA repair genes identified in D. radiodurans are present in sensitive bacteria, whereas the involvement of many uncharacterized genes implicatedmore » in resistance by transcriptome analyses has not been borne out by mutant studies. Genomic subtraction of D. geothermalis from D. radiodurans was used to define a minimal gene set for extreme resistance, whereby unique genes were ruled out, and shared genes were pooled as candidates for resistance. We revise down substantially the number of potential genetic determinants of extreme radiation resistance, identify a putative regulator and a palindromic binding site for genes which comprise a distinct Deinococcus radiation response regulon, and consider the impact of those findings on the prevailing models of extreme radiation resistance.« less
  • Deinococcus radiodurans is extremely resistant to ionizing radiation. How this bacterium can grow under chronic gamma-radiation (50 Gy/hour) or recover from acute doses greater than 10 kGy is unknown. We show that D. radiodurans accumulates very high intracellular manganese and low iron levels compared to radiation sensitive bacteria, and resistance exhibits a concentration-dependent response to Mn(II). Among the most radiation-resistant bacterial groups reported, Deinococcus, Enterococcus, Lactobacillus and cyanobacteria spp. accumulate Mn(II). In contrast, Shewanella oneidensis and Pseudomonas putida have high Fe but low intracellular Mn concentrations and are very sensitive. We propose that Mn(II) accumulation facilitates recovery from radiation injury.