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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 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. 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 emergedmore » 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:
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Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
Genomics Division
OSTI Identifier:
937567
Report Number(s):
LBNL-934E
DOE Contract Number:  
DE-AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
PLos One
Additional Journal Information:
Journal Volume: 2; Journal Issue: 9; Related Information: Journal Publication Date: September 2007
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Radiation Resistant Genes, Deinococcus geothermalis

Citation Formats

Makarova, Kira S, Omelchenko, Marina V, Gaidamakova, Elena K, Matrosova, Vera Y, Vasilenko, Alexander, Zhai, Min, Lapidus, Alla, Copeland, Alex, Kim, Edwin, Land, Miriam, Mavrommatis, Konstantinos, Pitluck, Samuel, Richardson, Paul M, Detter, Chris, Brettin, Thomas, Saunders, Elizabeth, Lai, Barry, Ravel, Bruce, Kemner, Kenneth M, Wolf, Yuri I, Sorokin, Alexander, Gerasimova, Anna V, Gelfand, Mikhail S, Fredrickson, James K, Koonin, Eugene V, and Daly, Michael J. 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 V, Gaidamakova, Elena K, Matrosova, Vera Y, Vasilenko, Alexander, Zhai, Min, Lapidus, Alla, Copeland, Alex, Kim, Edwin, Land, Miriam, Mavrommatis, Konstantinos, Pitluck, Samuel, Richardson, Paul M, Detter, Chris, Brettin, Thomas, Saunders, Elizabeth, Lai, Barry, Ravel, Bruce, Kemner, Kenneth M, Wolf, Yuri I, Sorokin, Alexander, Gerasimova, Anna V, Gelfand, Mikhail S, Fredrickson, James K, Koonin, Eugene V, & Daly, Michael J. Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks. United States. https://doi.org/10.1371/journal.pone.0000955
Makarova, Kira S, Omelchenko, Marina V, Gaidamakova, Elena K, Matrosova, Vera Y, Vasilenko, Alexander, Zhai, Min, Lapidus, Alla, Copeland, Alex, Kim, Edwin, Land, Miriam, Mavrommatis, Konstantinos, Pitluck, Samuel, Richardson, Paul M, Detter, Chris, Brettin, Thomas, Saunders, Elizabeth, Lai, Barry, Ravel, Bruce, Kemner, Kenneth M, Wolf, Yuri I, Sorokin, Alexander, Gerasimova, Anna V, Gelfand, Mikhail S, Fredrickson, James K, Koonin, Eugene V, and Daly, Michael J. 2007. "Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks". United States. https://doi.org/10.1371/journal.pone.0000955. https://www.osti.gov/servlets/purl/937567.
@article{osti_937567,
title = {Deinococcus geothermalis: The Pool of Extreme Radiation Resistance Genes Shrinks},
author = {Makarova, Kira S and Omelchenko, Marina V and Gaidamakova, Elena K and Matrosova, Vera Y and Vasilenko, Alexander and Zhai, Min and Lapidus, Alla and Copeland, Alex and Kim, Edwin and Land, Miriam and Mavrommatis, Konstantinos and Pitluck, Samuel and Richardson, Paul M and Detter, Chris and Brettin, Thomas and Saunders, Elizabeth and Lai, Barry and Ravel, Bruce and Kemner, Kenneth M and Wolf, Yuri I and Sorokin, Alexander and Gerasimova, Anna V and Gelfand, Mikhail S and Fredrickson, James K and Koonin, Eugene V and Daly, Michael J},
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 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. 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},
url = {https://www.osti.gov/biblio/937567}, journal = {PLos One},
number = 9,
volume = 2,
place = {United States},
year = {2007},
month = {7}
}