, Volume 108, Issue 1, pp 25–34

Specific Expansion of Protein Families in the Radioresistant Bacterium Deinococcus Radiodurans

  • Kira S. Makarova
  • L. Aravind
  • Michael J. Daly
  • Eugene V. Koonin


Computer analysis of the complete genome of Deinococcus radioduransR1 reveals a number of protein families, which are over-represented in this organism, compared to most other bacteria with known genome sequences. These families include both previously characterized and uncharacterized proteins. Most of the families whose functions are known or could be predicted seem to be related to stress-response and elimination of damage products (cell-cleaning). The two most prominent family expansions are the Nudix (MutT) family of pyrophosphohydrolases and a previously unnoticed family of proteins related to Bacillus subtilisDinB that could possess a metal-dependent enzymatic activity whose exact nature remains to be determined. Several proteins of the expanded families, particularly the Nudix family, are fused to other domains and form multidomain proteins that are so far unique for Deinococcus. The domain composition of some of these proteins indicates that they could be involved in novel DNA-repair pathways. Such unique proteins are good targets for knock-out and gene expression studies, which are aimed to shed light on the unusual features of this interesting10.6pt bacterium.

Deinococcus genome analysis protein family specific expansion 


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  1. 1.
    Alexander D. et al.: Increased tolerance to two oomycete pathogens in transgenic tobacco expressing pathogenesisrelated protein 1a, Proc. Natl. Acad. Sci. USA 90(1993): 7327–7331.Google Scholar
  2. 2.
    Altschul S.F. et al.: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucleic Acids Res. 25(1997): 3389–3402.Google Scholar
  3. 3.
    Antelmann H. et al.: First steps from a two-dimensional protein index towards a response-regulation map for Bacillus subtilis, Electrophoresis 18(1997): 1451–1463.Google Scholar
  4. 4.
    Azeddoug H. and Reysset G.: Cloning and sequencing of a chromosomal fragment from Clostridium acetobutylicum strain ABKn8 conferring chemical-damaging agents and UV resistance to E. colirecA strains, Curr. Microbiol. 29(1994): 229–235.Google Scholar
  5. 5.
    Battista J.R.: Against all odds: the survival strategies of Deinococcus radiodurans, Annu. Rev. Microbiol. 51(1997): 203–224.Google Scholar
  6. 6.
    Battista J.R., Earl A.M. and Park M.J.:Why is deinococcus radiodurans so resistant to ionizing radiation? Trends Microbiol. 7(1999): 362–365.Google Scholar
  7. 7.
    Bessman M.J., Frick D.N. and O'Handley S.F.: The MutT proteins or ‘Nudix’ hydrolases, a family of versatile, widely distributed, ‘housecleaning’ enzymes, J. Biol. Chem. 271(1996): 25059–25062.Google Scholar
  8. 8.
    Cheo D.L., Bayles K.W. and Yasbin R.E.: Cloning and characterization of DNA damage-inducible promoter regions from Bacillus subtilis, J. Bacteriol. 173(1991): 1696–1703.Google Scholar
  9. 9.
    Chervitz S.A. et al.: Comparison of the complete protein sets of worm and yeast: orthology and divergence, Science 282(1998): 2022–2028.Google Scholar
  10. 10.
    Cole S.T. et al.: Deciphering the biology of Mycobacterium tuberculosisfrom the complete genome sequence, Nature 393(1998): 537–544.Google Scholar
  11. 11.
    Diorio C. et al.: An Escherichia colichromosomal ars operon homolog is functional in arsenic detoxification and is conserved in gram-negative bacteria, J. Bacteriol. 177(1995): 2050–2056.Google Scholar
  12. 12.
    Fernandez C. et al.: NMR solution structure of the pathogenesis-related protein P14a, J. Mol. Biol. 266(1997): 576–593.Google Scholar
  13. 13.
    Fujimori A. et al.: Cloning and mapping of Np95 gene which encodes a novel nuclear protein associated with cell proliferation, Mamm. Genome 9(1998): 1032–1035.Google Scholar
  14. 14.
    Grant C.E., Bain G. and Tsang A.: The molecular basis for alternative splicing of the CABP1 transcripts in Dictyostelium discoideum, Nucleic Acids Res. 18(1990): 5457–5463.Google Scholar
  15. 15.
    Hecht H.J. et al.: The metal-ion-free oxidoreductase from Streptomyces aureofaciens has an alpha/beta hydrolase fold, Nat. Struct. Biol. 1(1994): 532–537.Google Scholar
  16. 16.
    Hiom K. and Sedgwick S.G.: Cloning and structural characterization of the mcrA locus of Escherichia coli, J. Bacteriol. 173(1991): 7368–7373.Google Scholar
  17. 17.
    Jobling M.G. and Ritchie D.A.: The nucleotide sequence of a plasmid determinant for resistance to tellurium anions, Gene 66: 245–258.Google Scholar
  18. 18.
    Koonin E.V.: A highly conserved sequence motif defining the family of MutT-related proteins from eubacteria, eukaryotes and viruses, Nucleic Acids Res. 21(1993): 4847.Google Scholar
  19. 19.
    Kunst F. et al.: The complete genome sequence of the grampositive bacterium Bacillus subtilis, Nature 390(1997): 249–256.Google Scholar
  20. 20.
    Lange C.C. et al.: Engineering a recombinant Deinococcus radiodurans for organopollutant degradation in radioactive mixed waste environments, Nat Biotechnol 16(1998): 929–933.Google Scholar
  21. 21.
    Linthorst H.J. et al.: Tobacco and tomato PR proteins homologous to win and pro-hevein lack the ‘hevein’ domain, Mol. Plant Microbe. Interact. 4(1991): 586–592.Google Scholar
  22. 22.
    Makarova K.S et al.: Comparative genomics of the Archaea (Euryarchaeota): evolution of conserved protein families, the stable core, and the variable shell, Genome Res. 9(1999): 608–628.Google Scholar
  23. 23.
    Mattimore V. and Battista J.R.: Radioresistance of Deinococcus radiodurans: functions necessary to survive ionizing radiation are also necessary to survive prolonged desiccation, J. Bacteriol. 178(1996): 633–637.Google Scholar
  24. 24.
    Minton K.W. and Daly M.J.: A model for repair of radiationinduced DNA double-strand breaks in the extreme radiophile Deinococcus radiodurans, Bioessays 17(1995): 457–464.Google Scholar
  25. 25.
    Myers C.R. and Myers J.M.: Outer membrane cytochromes of Shewanella putrefaciens MR-1: spectral analysis, and purification of the 83-kDa c-type cytochrome, Biochim. Biophys. Acta 1326(1997): 307–318.Google Scholar
  26. 26.
    Raibaud A. et al.: Nucleotide sequence analysis reveals linked N-acetyl hydrolase, thioesterase, transport, and regulatory genes encoded by the bialaphos biosynthetic gene cluster of Streptomyces hygroscopicus, J. Bacteriol. 173(1991): 4454–4463.Google Scholar
  27. 27.
    Rathbone D.A. et al.: Molecular analysis of the Rhodococcus sp. strain H1 her gene and characterization of its product, a heroin esterase, expressed in Escherichia coli, Appl. Environ. Microbiol. 63(1997): 2062–2066.Google Scholar
  28. 28.
    Schaffer A.A. et al.: IMPALA: Matching a protein sequence against a collection of PSI-BLAST-constructed positionspecific score matrices, Bioinformatics(2000) (in press).Google Scholar
  29. 29.
    Schlenk D.: Occurrence of flavin-containing monooxygenases in non-mammalian eukaryotic organisms, Comp. Biochem. Physiol. C Pharmacol. Toxicol. Endocrinol. 121(1998): 185–195.Google Scholar
  30. 30.
    Seledtsov I.A., Vul'f Iu. I. and Makarova K.S.: Multiple alignment of biopolymer sequences, based on the search for statistically significant common segments, Mol. Biol. (Mosk) 29(1995): 1023–1039.Google Scholar
  31. 31.
    Smith M.D. et al.: Duplication insertion of drug resistance determinants in the radioresistant bacterium Deinococcus radiodurans, J. Bacteriol. 170(1988): 2126–2135.Google Scholar
  32. 32.
    Stephens R.S. et al.: Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis, Science 282(1998): 754–759.Google Scholar
  33. 33.
    Thelwell C., Robinson N.J. and Turner-Cavet J.S.: An SmtBlike repressor from Synechocystis PCC 6803 regulates a zinc exporter, Proc. Natl. Acad. Sci. USA 95(1998): 10728–10733.Google Scholar
  34. 34.
    Udupa K.S. et al.: Novel ionizing radiation-sensitive mutants of Deinococcus radiodurans, J. Bacteriol. 176(1994): 7439–7446.Google Scholar
  35. 35.
    Walker D.R. and E.V. Koonin: SEALS: a system for easy analysis of lots of sequences, Ismb 5(1997): 333–339.Google Scholar
  36. 36.
    White O. et al.: Genome Sequence of the Radioresistant Bacterium Deinococcus radiodurans R1, Science 286(1999): 1571–1577.Google Scholar
  37. 37.
    Wolf Y.I. et al.: Distribution of protein folds in the three superkingdoms of life, Genome Res. 9(1999): 17–26.Google Scholar
  38. 38.
    Wootton J.C.: Non-globular domains in protein sequences: automated segmentation using complexity measures, Comput. Chem. 18(1994): 269–285.Google Scholar
  39. 39.
    Yamamoto M et al.: Cloning and sequencing of a 35.7 kb in the 70 degree-73 degree region of the Bacillus subtilis genome reveal genes for a new two-component system, three spore germination proteins, an iron uptake system and a general stress response protein, Gene 194(1997): 191–199.Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Kira S. Makarova
    • 1
    • 2
    • 3
  • L. Aravind
    • 2
  • Michael J. Daly
    • 1
  • Eugene V. Koonin
    • 2
  1. 1.Uniformed Services University of the Health SciencesBethesdaUSA
  2. 2.The National Institutes of HealthThe National Center for Biotechnology Information National Library of MedicineBethesdaUSA
  3. 3.Institute of Cytology and GeneticsRussian Academy of SciencesNovosibirskRussia

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