This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Makarova, K. S.
Right arrow Articles by Daly, M. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Makarova, K. S.
Right arrow Articles by Daly, M. J.

 Previous Article  |  Next Article 

Microbiology and Molecular Biology Reviews, March 2001, p. 44-79, Vol. 65, No. 1
1092-2172/01/$04.00+0   DOI: 10.1128/MMBR.65.1.44-79.2001

Genome of the Extremely Radiation-Resistant Bacterium Deinococcus radiodurans Viewed from the Perspective of Comparative Genomics

Kira S. Makarova,1,2 L. Aravind,2 Yuri I. Wolf,2 Roman L. Tatusov,2 Kenneth W. Minton,1 Eugene V. Koonin,2 and Michael J. Daly1,*

Uniformed Services University of the Health Sciences, Bethesda, Maryland 20814-4799,1 and National Center for Biotechnology Information, National Institutes of Health, Bethesda, Maryland 208142

The bacterium Deinococcus radiodurans shows remarkable resistance to a range of damage caused by ionizing radiation, desiccation, UV radiation, oxidizing agents, and electrophilic mutagens. D. radiodurans is best known for its extreme resistance to ionizing radiation; not only can it grow continuously in the presence of chronic radiation (6 kilorads/h), but also it can survive acute exposures to gamma radiation exceeding 1,500 kilorads without dying or undergoing induced mutation. These characteristics were the impetus for sequencing the genome of D. radiodurans and the ongoing development of its use for bioremediation of radioactive wastes. Although it is known that these multiple resistance phenotypes stem from efficient DNA repair processes, the mechanisms underlying these extraordinary repair capabilities remain poorly understood. In this work we present an extensive comparative sequence analysis of the Deinococcus genome. Deinococcus is the first representative with a completely sequenced genome from a distinct bacterial lineage of extremophiles, the Thermus-Deinococcus group. Phylogenetic tree analysis, combined with the identification of several synapomorphies between Thermus and Deinococcus, supports the hypothesis that it is an ancient group with no clear affinities to any of the other known bacterial lineages. Distinctive features of the Deinococcus genome as well as features shared with other free-living bacteria were revealed by comparison of its proteome to the collection of clusters of orthologous groups of proteins. Analysis of paralogs in Deinococcus has revealed several unique protein families. In addition, specific expansions of several other families including phosphatases, proteases, acyltransferases, and Nudix family pyrophosphohydrolases were detected. Genes that potentially affect DNA repair and recombination and stress responses were investigated in detail. Some proteins appear to have been horizontally transferred from eukaryotes and are not present in other bacteria. For example, three proteins homologous to plant desiccation resistance proteins were identified, and these are particularly interesting because of the correlation between desiccation and radiation resistance. Compared to other bacteria, the D. radiodurans genome is enriched in repetitive sequences, namely, IS-like transposons and small intergenic repeats. In combination, these observations suggest that several different biological mechanisms contribute to the multiple DNA repair-dependent phenotypes of this organism.


* Corresponding author. Mailing address: Department of Pathology, Room B3153, Uniformed Services University of the Health Sciences, 4301 Jones Bridge Rd., Bethesda, MD 20814-4799. Phone: (301) 295-3750. Fax: (301) 295-1640. E-mail: mdaly{at}usuhs.mil.


Microbiology and Molecular Biology Reviews, March 2001, p. 44-79, Vol. 65, No. 1
1092-2172/01/$04.00+0   DOI: 10.1128/MMBR.65.1.44-79.2001



This article has been cited by other articles:

  • Yuan, M., Zhang, W., Dai, S., Wu, J., Wang, Y., Tao, T., Chen, M., Lin, M. (2009). Deinococcus gobiensis sp. nov., an extremely radiation-resistant bacterium. Int. J. Syst. Evol. Microbiol. 59: 1513-1517 [Abstract] [Full Text]  
  • Lieber, A., Leis, A., Kushmaro, A., Minsky, A., Medalia, O. (2009). Chromatin Organization and Radio Resistance in the Bacterium Gemmata obscuriglobus. J. Bacteriol. 191: 1439-1445 [Abstract] [Full Text]  
  • Lu, H., Gao, G., Xu, G., Fan, L., Yin, L., Shen, B., Hua, Y. (2009). Deinococcus radiodurans PprI Switches on DNA Damage Response and Cellular Survival Networks after Radiation Damage. Mol. Cell. Proteomics 8: 481-494 [Abstract] [Full Text]  
  • Luo, S., Levine, R. L. (2009). Methionine in proteins defends against oxidative stress. FASEB J. 23: 464-472 [Abstract] [Full Text]  
  • Makharashvili, N., Mi, T., Koroleva, O., Korolev, S. (2009). RecR-mediated Modulation of RecF Dimer Specificity for Single- and Double-stranded DNA. J. Biol. Chem. 284: 1425-1434 [Abstract] [Full Text]  
  • Tian, B., Sun, Z., Xu, Z., Shen, S., Wang, H., Hua, Y. (2008). Carotenoid 3',4'-desaturase is involved in carotenoid biosynthesis in the radioresistant bacterium Deinococcus radiodurans. Microbiology 154: 3697-3706 [Abstract] [Full Text]  
  • Koonin, E. V., Wolf, Y. I. (2008). Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world. Nucleic Acids Res 36: 6688-6719 [Abstract] [Full Text]  
  • Rajpurohit, Y. S., Gopalakrishnan, R., Misra, H. S. (2008). Involvement of a Protein Kinase Activity Inducer in DNA Double Strand Break Repair and Radioresistance of Deinococcus radiodurans. J. Bacteriol. 190: 3948-3954 [Abstract] [Full Text]  
  • Mendell, J. E., Clements, K. D., Choat, J. H., Angert, E. R. (2008). From the Cover: Extreme polyploidy in a large bacterium. Proc. Natl. Acad. Sci. USA 105: 6730-6734 [Abstract] [Full Text]  
  • Xu, G., Wang, L., Chen, H., Lu, H., Ying, N., Tian, B., Hua, Y. (2008). RecO Is Essential for DNA Damage Repair in Deinococcus radiodurans. J. Bacteriol. 190: 2624-2628 [Abstract] [Full Text]  
  • Bentchikou, E., Servant, P., Coste, G., Sommer, S. (2007). Additive Effects of SbcCD and PolX Deficiencies in the In Vivo Repair of DNA Double-Strand Breaks in Deinococcus radiodurans. J. Bacteriol. 189: 4784-4790 [Abstract] [Full Text]  
  • Xu, Z., Tian, B., Sun, Z., Lin, J., Hua, Y. (2007). Identification and functional analysis of a phytoene desaturase gene from the extremely radioresistant bacterium Deinococcus radiodurans. Microbiology 153: 1642-1652 [Abstract] [Full Text]  
  • Heinz, K., Marx, A. (2007). Lesion Bypass Activity of DNA Polymerase A from the Extremely Radioresistant Organism Deinococcus radiodurans. J. Biol. Chem. 282: 10908-10914 [Abstract] [Full Text]  
  • Satoh, K., Ohba, H., Sghaier, H., Narumi, I. (2006). Down-regulation of radioresistance by LexA2 in Deinococcus radiodurans.. Microbiology 152: 3217-3226 [Abstract] [Full Text]  
  • Drapeau, M. D., Albert, S., Kucharski, R., Prusko, C., Maleszka, R. (2006). Evolution of the Yellow/Major Royal Jelly Protein family and the emergence of social behavior in honey bees. Genome Res 16: 1385-1394 [Abstract] [Full Text]  
  • Saarimaa, C., Peltola, M., Raulio, M., Neu, T. R., Salkinoja-Salonen, M. S., Neubauer, P. (2006). Characterization of Adhesion Threads of Deinococcus geothermalis as Type IV Pili.. J. Bacteriol. 188: 7016-7021 [Abstract] [Full Text]  
  • Minsky, A., Shimoni, E., Englander, J. (2006). Ring-Like Nucleoids and DNA Repair through Error-Free Nonhomologous End Joining in Deinococcus radiodurans.. J. Bacteriol. 188: 6047-6051 [Full Text]  
  • Brim, H., Osborne, J. P., Kostandarithes, H. M., Fredrickson, J. K., Wackett, L. P., Daly, M. J. (2006). Deinococcus radiodurans engineered for complete toluene degradation facilitates Cr(VI) reduction.. Microbiology 152: 2469-2477 [Abstract] [Full Text]  
  • Killoran, M. P., Keck, J. L. (2006). Three HRDC Domains Differentially Modulate Deinococcus radiodurans RecQ DNA Helicase Biochemical Activity. J. Biol. Chem. 281: 12849-12857 [Abstract] [Full Text]  
  • Qiu, X., Daly, M. J., Vasilenko, A., Omelchenko, M. V., Gaidamakova, E. K., Wu, L., Zhou, J., Sundin, G. W., Tiedje, J. M. (2006). Transcriptome Analysis Applied to Survival of Shewanella oneidensis MR-1 Exposed to Ionizing Radiation. J. Bacteriol. 188: 1199-1204 [Abstract] [Full Text]  
  • Bik, E. M., Eckburg, P. B., Gill, S. R., Nelson, K. E., Purdom, E. A., Francois, F., Perez-Perez, G., Blaser, M. J., Relman, D. A. (2006). Molecular analysis of the bacterial microbiota in the human stomach. Proc. Natl. Acad. Sci. USA 103: 732-737 [Abstract] [Full Text]  
  • D'Errico, G., Di Salle, A., La Cara, F., Rossi, M., Cannio, R. (2006). Identification and Characterization of a Novel Bacterial Sulfite Oxidase with No Heme Binding Domain from Deinococcus radiodurans. J. Bacteriol. 188: 694-701 [Abstract] [Full Text]  
  • Moe, E., Leiros, I., Smalas, A. O., McSweeney, S. (2006). The Crystal Structure of Mismatch-specific Uracil-DNA Glycosylase (MUG) from Deinococcus radiodurans Reveals a Novel Catalytic Residue and Broad Substrate Specificity. J. Biol. Chem. 281: 569-577 [Abstract] [Full Text]  
  • Barabote, R. D., Saier, M. H. Jr. (2005). Comparative Genomic Analyses of the Bacterial Phosphotransferase System. Microbiol. Mol. Biol. Rev. 69: 608-634 [Abstract] [Full Text]  
  • de Groot, A., Chapon, V., Servant, P., Christen, R., Saux, M. F.-L., Sommer, S., Heulin, T. (2005). Deinococcus deserti sp. nov., a gamma-radiation-tolerant bacterium isolated from the Sahara Desert. Int. J. Syst. Evol. Microbiol. 55: 2441-2446 [Abstract] [Full Text]  
  • Alpert, P. (2005). The Limits and Frontiers of Desiccation-Tolerant Life. Integr. Comp. Biol. 45: 685-695 [Abstract] [Full Text]  
  • Ciccarelli, F. D., Bork, P. (2005). The WHy domain mediates the response to desiccation in plants and bacteria. Bioinformatics 21: 1304-1307 [Abstract] [Full Text]  
  • Blondal, T., Hjorleifsdottir, S., Aevarsson, A., Fridjonsson, O. H., Skirnisdottir, S., Wheat, J. O., Hermannsdottir, A. G., Hreggvidsson, G. O., Smith, A. V., Kristjansson, J. K. (2005). Characterization of a 5'-Polynucleotide Kinase/3'-Phosphatase from Bacteriophage RM378. J. Biol. Chem. 280: 5188-5194 [Abstract] [Full Text]  
  • Martins, A., Shuman, S. (2004). An RNA Ligase from Deinococcus radiodurans. J. Biol. Chem. 279: 50654-50661 [Abstract] [Full Text]  
  • Wilkinson, S. P., Grove, A. (2004). HucR, a Novel Uric Acid-responsive Member of the MarR Family of Transcriptional Regulators from Deinococcus radiodurans. J. Biol. Chem. 279: 51442-51450 [Abstract] [Full Text]  
  • Kulbachinskiy, A., Bass, I., Bogdanova, E., Goldfarb, A., Nikiforov, V. (2004). Cold Sensitivity of Thermophilic and Mesophilic RNA Polymerases. J. Bacteriol. 186: 7818-7820 [Abstract] [Full Text]  
  • Daly, M. J., Gaidamakova, E. K., Matrosova, V. Y., Vasilenko, A., Zhai, M., Venkateswaran, A., Hess, M., Omelchenko, M. V., Kostandarithes, H. M., Makarova, K. S., Wackett, L. P., Fredrickson, J. K., Ghosal, D. (2004). Accumulation of Mn(II) in Deinococcus radiodurans Facilitates Gamma-Radiation Resistance. Science 306: 1025-1028 [Abstract] [Full Text]  
  • Englander, J., Klein, E., Brumfeld, V., Sharma, A. K., Doherty, A. J., Minsky, A. (2004). DNA Toroids: Framework for DNA Repair in Deinococcus radiodurans and in Germinating Bacterial Spores. J. Bacteriol. 186: 5973-5977 [Full Text]  
  • Tanaka, M., Earl, A. M., Howell, H. A., Park, M.-J., Eisen, J. A., Peterson, S. N., Battista, J. R. (2004). Analysis of Deinococcus radiodurans's Transcriptional Response to Ionizing Radiation and Desiccation Reveals Novel Proteins That Contribute to Extreme Radioresistance. Genetics 168: 21-33 [Abstract] [Full Text]  
  • Meunier-Jamin, C., Kapp, U., Leonard, G. A., McSweeney, S. (2004). The Structure of the Organic Hydroperoxide Resistance Protein from Deinococcus radiodurans: DO CONFORMATIONAL CHANGES FACILITATE RECYCLING OF THE REDOX DISULFIDE?. J. Biol. Chem. 279: 25830-25837 [Abstract] [Full Text]  
  • Bernstein, D. A., Eggington, J. M., Killoran, M. P., Misic, A. M., Cox, M. M., Keck, J. L. (2004). Crystal structure of the Deinococcus radiodurans single-stranded DNA-binding protein suggests a mechanism for coping with DNA damage. Proc. Natl. Acad. Sci. USA 101: 8575-8580 [Abstract] [Full Text]  
  • Griffiths, E., Gupta, R. S. (2004). Distinctive Protein Signatures Provide Molecular Markers and Evidence for the Monophyletic Nature of the Deinococcus-Thermus Phylum. J. Bacteriol. 186: 3097-3107 [Abstract] [Full Text]  
  • Givens, R. M., Lin, M.-H., Taylor, D. J., Mechold, U., Berry, J. O., Hernandez, V. J. (2004). Inducible Expression, Enzymatic Activity, and Origin of Higher Plant Homologues of Bacterial RelA/SpoT Stress Proteins in Nicotiana tabacum. J. Biol. Chem. 279: 7495-7504 [Abstract] [Full Text]  
  • Haruta, N., Yu, X., Yang, S., Egelman, E. H., Cox, M. M. (2003). A DNA Pairing-enhanced Conformation of Bacterial RecA Proteins. J. Biol. Chem. 278: 52710-52723 [Abstract] [Full Text]  
  • Brim, H., Venkateswaran, A., Kostandarithes, H. M., Fredrickson, J. K., Daly, M. J. (2003). Engineering Deinococcus geothermalis for Bioremediation of High-Temperature Radioactive Waste Environments. Appl. Environ. Microbiol. 69: 4575-4582 [Abstract] [Full Text]  
  • Klotz, M. G., Loewen, P. C. (2003). The Molecular Evolution of Catalatic Hydroperoxidases: Evidence for Multiple Lateral Transfer of Genes Between Prokaryota and from Bacteria into Eukaryota. Mol Biol Evol 20: 1098-1112 [Abstract] [Full Text]  
  • Goyal, K., Tisi, L., Basran, A., Browne, J., Burnell, A., Zurdo, J., Tunnacliffe, A. (2003). Transition from Natively Unfolded to Folded State Induced by Desiccation in an Anhydrobiotic Nematode Protein. J. Biol. Chem. 278: 12977-12984 [Abstract] [Full Text]  
  • Liu, Y., Zhou, J., Omelchenko, M. V., Beliaev, A. S., Venkateswaran, A., Stair, J., Wu, L., Thompson, D. K., Xu, D., Rogozin, I. B., Gaidamakova, E. K., Zhai, M., Makarova, K. S., Koonin, E. V., Daly, M. J. (2003). Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl. Acad. Sci. USA 100: 4191-4196 [Abstract] [Full Text]  
  • Levin-Zaidman, S., Englander, J., Shimoni, E., Sharma, A. K., Minton, K. W., Minsky, A. (2003). Ringlike Structure of the Deinococcus radiodurans Genome: A Key to Radioresistance?. Science 299: 254-256 [Abstract] [Full Text]  
  • Earl, A. M., Mohundro, M. M., Mian, I. S., Battista, J. R. (2002). The IrrE Protein of Deinococcus radiodurans R1 Is a Novel Regulator of recA Expression. J. Bacteriol. 184: 6216-6224 [Abstract] [Full Text]  
  • Southworth, M. W., Perler, F. B. (2002). Protein Splicing of the Deinococcus radiodurans Strain R1 Snf2 Intein. J. Bacteriol. 184: 6387-6388 [Abstract] [Full Text]  
  • Taylor, D. E., Rooker, M., Keelan, M., Ng, L.-K., Martin, I., Perna, N. T., Burland, N. T. V., Blattner, F. R. (2002). Genomic Variability of O Islands Encoding Tellurite Resistance in Enterohemorrhagic Escherichia coli O157:H7 Isolates. J. Bacteriol. 184: 4690-4698 [Abstract] [Full Text]  
  • Nishida, H., Narumi, I. (2002). Disruption analysis of DR1420 and/or DR1758 in the extremely radioresistant bacterium Deinococcus radiodurans. Microbiology 148: 2911-2914 [Abstract] [Full Text]  
  • Mrazek, J. (2002). New technology may reveal mechanisms of radiation resistance in Deinococcus radiodurans. Proc. Natl. Acad. Sci. USA 99: 10943-10944 [Full Text]  
  • Lipton, M. S., Pasa-Tolic', L., Anderson, G. A., Anderson, D. J., Auberry, D. L., Battista, J. R., Daly, M. J., Fredrickson, J., Hixson, K. K., Kostandarithes, H., Masselon, C., Markillie, L. M., Moore, R. J., Romine, M. F., Shen, Y., Stritmatter, E., Tolic', N., Udseth, H. R., Venkateswaran, A., Wong, K.-K., Zhao, R., Smith, R. D. (2002). From the Cover: Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags. Proc. Natl. Acad. Sci. USA 99: 11049-11054 [Abstract] [Full Text]  
  • Kim, J.-I., Cox, M. M. (2002). The RecA proteins of Deinococcus radiodurans and Escherichia coli promote DNA strand exchange via inverse pathways. Proc. Natl. Acad. Sci. USA 99: 7917-7921 [Abstract] [Full Text]  
  • Kolari, M., Schmidt, U., Kuismanen, E., Salkinoja-Salonen, M. S. (2002). Firm but Slippery Attachment of Deinococcus geothermalis. J. Bacteriol. 184: 2473-2480 [Abstract] [Full Text]  
  • Slesarev, A. I., Mezhevaya, K. V., Makarova, K. S., Polushin, N. N., Shcherbinina, O. V., Shakhova, V. V., Belova, G. I., Aravind, L., Natale, D. A., Rogozin, I. B., Tatusov, R. L., Wolf, Y. I., Stetter, K. O., Malykh, A. G., Koonin, E. V., Kozyavkin, S. A. (2002). The complete genome of hyperthermophile Methanopyrus kandleri AV19 and monophyly of archaeal methanogens. Proc. Natl. Acad. Sci. USA 99: 4644-4649 [Abstract] [Full Text]  
  • Kim, J.-I., Sharma, A. K., Abbott, S. N., Wood, E. A., Dwyer, D. W., Jambura, A., Minton, K. W., Inman, R. B., Daly, M. J., Cox, M. M. (2002). RecA Protein from the Extremely Radioresistant Bacterium Deinococcus radiodurans: Expression, Purification, and Characterization. J. Bacteriol. 184: 1649-1660 [Abstract] [Full Text]  
  • Earl, A. M., Rankin, S. K., Kim, K.-P., Lamendola, O. N., Battista, J. R. (2002). Genetic Evidence that the uvsE Gene Product of Deinococcus radiodurans R1 Is a UV Damage Endonuclease. J. Bacteriol. 184: 1003-1009 [Abstract] [Full Text]  
  • Narumi, I., Satoh, K., Kikuchi, M., Funayama, T., Yanagisawa, T., Kobayashi, Y., Watanabe, H., Yamamoto, K. (2001). The LexA Protein from Deinococcus radiodurans Is Not Involved in RecA Induction following gamma Irradiation. J. Bacteriol. 183: 6951-6956 [Abstract] [Full Text]  
  • Li, X., Lu, A-L. (2001). Molecular Cloning and Functional Analysis of the MutY Homolog of Deinococcus radiodurans. J. Bacteriol. 183: 6151-6158 [Abstract] [Full Text]  
  • Miyazaki, J., Kobashi, N., Nishiyama, M., Yamane, H. (2001). Functional and Evolutionary Relationship between Arginine Biosynthesis and Prokaryotic Lysine Biosynthesis through {alpha}-Aminoadipate. J. Bacteriol. 183: 5067-5073 [Abstract] [Full Text]  
  • Krogh, B. O., Shuman, S. (2002). A poxvirus-like type IB topoisomerase family in bacteria. Proc. Natl. Acad. Sci. USA 99: 1853-1858 [Abstract] [Full Text]