Physiological and molecular basis of extreme radioresistance in Deinococcus radiodurans

Current Science

Volumn 104, Issue 2, 2013, Pages 194-205

  Misra, H S ^a   Rajpurohit, Y S ^a   Kota, Swathi ^a  

^a BHABHA ATOMIC RESEARCH CENTRE   (India)

Author keywords

Deinococcus radiodurans; DNA damage response; Extreme radio resistance; Oxidative stress tolerance

Indexed keywords

EID: 84874685092     PISSN: 00113891     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (104)

1. Blasius, M., Sommer, S. and Hubscher, U., Deinococcus radiodurans: what belongs to the survival kit Crit. Rev. Biochem. Mol. Biol., 2008, 43, 221-238.
2. Slade, D. and Radman, M., Oxidative stress resistance in Deinococcus radiodurans. Microbiol. Mol. Biol. Rev., 2011, 75, 133- 191.
3. Anderson, A. W., Nordan, H. C., Cain, R. F., Parrish, G. and Duggan, D., Studies on a radioresistant Micrococcus: isolation, morphology, cultural characteristics, and resistance to gamma radiation. Food Technol., 1956, 10, 575-577.
4. Englander, J., Klein, E., Brumfeld, V., Sharma, A. K., Doherty, A. J. and Minsky, A., DNA toroids: framework for DNA repair in Deinococcus radiodurans and in germinating bacterial spores. J. Bacteriol., 2004, 186, 5973-5977.
5. Baumeister, W., Kubler, O. and Zingsheim, H. P., The structure of the cell envelope of Micrococcus radiodurans as revealed by metal shadowing and decoration. J. Ultrastruct. Res., 1981, 75, 60-71.
6. Thompson, B. G. and Murray, R. G. E., The association of the surface array and the outer membrane of Deinococcus radiodurans. Can. J. Microbiol., 1982, 28, 1081-1088.
7. Sleytr, U. B., Kocur, M., Glauert, A. M. and Thornley, M. J., A study by freeze-etching of the fine structure of Micrococcus radiodurans. Arch. Microbiol., 1973, 94, 77-87.
8. Smith, M. D., Abrahamson, R. and Minton, K. W., Shuttle plasmids constructed by the transformation of an Escherichia coli cloning vector into two Deinococcus radiodurans plasmids. Plasmid, 1989, 22, 132-142.
9. Masters, C. I. and Minton, K. W., Promoter probe and shuttle plasmids for Deinococcus radiodurans. Plasmid, 1992, 26, 258- 261.
10. Tian, B., Xu, Z., Sun, Z., Lin, J. and Hua, Y., Evaluation of the antioxidant effects of carotenoids from Deinococcus radiodurans through targeted mutagenesis, chemiluminescence, and DNA damage analyses. Biochim. Biophys. Acta, 2007, 1770, 902-911.
11. Zhang, L., Yang, Q., Luo, X., Fang, C., Zhang, Q. and Tang, Y., Knockout of crtB or crtI gene blocks the carotenoid biosynthetic pathway in Deinococcus radiodurans R1 and influences its resistance to oxidative DNA-damaging agents due to change of free radicals scavenging ability. Arch. Microbiol., 2007, 188, 411-419.
12. Battista, J. R., Radiation resistance: the fragments that remain. Curr. Biol., 2000, 10, R204-R205.
13. 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., 1996, 178, 633-637.
14. Mattimore, V., Udupa, K. S., Berne, G. A. and Battista, J. R., Genetic characterization of forty ionizing radiation-sensitive strains of Deinococcus radiodurans: linkage information from transformation. J. Bacteriol., 1995, 177, 5232-5237.
15. Caimi, P. and Eisenstark, A., Sensitivity of Deinococcus radiodurans to near-ultraviolet radiation. Mutat. Res., 1986, 162, 145- 151.
16. Yasui, A. and McCready, S. J., Alternative repair pathways for UV-induced DNA damage. BioEssays, 1998, 20, 291-297.
17. Makarova, K. S., Aravind, L., Wolf, Y. I., Tatusov, R. L., Minton, K. W., Koonin, E. V. and Daly, M. J., Genome of the extremely radiation-resistant bacterium Deinococcus radiodurans viewed from the perspective of comparative genomics. Microbiol. Mol. Biol. Rev., 2001, 65, 44-79.
18. Earl, A. M., Rankin, S. K., Kim, K. P., Lamendola, O. N. and Battista, J. R., Genetic evidence that the uvsE gene product of Deinococcus radiodurans R1 is a UV damage endonuclease. J. Bacteriol., 2002, 184, 1003-1009.
19. Bauche, C. and Laval, J., Repair of oxidized bases in the extremely radiation resistant bacterium, Deinococcus radiodurans. J. Bacteriol., 1999, 181, 262-269.
20. Lecointe, F., Shevelev, I. V., Bailone, A., Sommer, S. and Hübscher, U., Involvement of an X family DNA polymerase in double-stranded break repair in the radioresistant organism Deinococcus radiodurans. Mol. Microbiol., 2004, 53, 1721-1730.
21. Khairnar, N. P. and Misra, H. S., DNA polymerase X from Deinococcus radiodurans implicated in bacterial tolerance to DNA damage is characterized as a short patch base excision repair polymerase. Microbiology, 2009, 155, 3005-3014.
22. Kota, S., Kamble, V. A., Rajpurohit, Y. S. and Misra, H. S., ATPtype DNA ligase requires other proteins for its activity in vitro and its operon components for radiation resistance in Deinococcus radiodurans in vivo. Biochem. Cell Biol., 2010, 88, 783-790.
23. Mennecier, S., Coste, G., Servant, P., Bailone, A. and Sommer, S., Mismatch repair ensures fidelity of replication and recombination in the radioresistant organism Deinococcus radiodurans. Mol. Genet. Genomics, 2004, 272, 460-469.
24. Moe, E., Leiros, I., Smalas, A. O. and McSweeney, S., 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., 2006, 281, 569- 577.
25. White, O. et al., Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1. Science, 1999, 286, 1571-1577.
26. Makarova, K. S. et al., Deinococcus geothermalis: the pool of extreme radiation resistance genes shrinks. PLoS One, 2007, 9, e955.
27. de Groot, A. et al., Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti. PLOS Genet., 2009, 5, e1000434.
28. Pukall, R. et al., Complete genome sequence of Deinococcus maricopensis type strain (LB-34). Stand. Genomic Sci., 2011, 4, 163-172.
29. Hua, Y., Narumi, I., Gao, G., Tian, B., Satoh, K., Kitayama, S. and Shen, B., PprI: a general switch responsible for extreme radioresistance of Deinococcus radiodurans. Biochem. Biophys. Res. Commun., 2003, 306, 354-360.
30. Narumi, I., Satoh, K., Cui, S., Funayama, T., Kitayama, S. and Watanabe, H., PprA: a novel protein from Deinococcus radiodurans that stimulates DNA ligation. Mol. Microbiol., 2004, 54, 278-285.
31. Sghaier, H., Ghedira, K., Benkahla, A. and Barkallah, I., Basal DNA repair machinery is subject to positive selection in ionizingradiation-resistant bacteria. BMC Genomics, 2008, 9, 297.
32. Daly, M. J. and Minton, K. W., An alternative pathway of recombination of chromosomal fragments precedes recA-dependent recombination in the radioresistant bacterium Deinococcus radiodurans. J. Bacteriol., 1996, 178, 4461-4471.
33. Wang, J. and Julin, D. A., DNA helicase activity of the RecD protein from Deinococcus radiodurans. J. Biol. Chem., 2004, 279, 52024-52032.
34. Khairnar, N. P., Kamble, V. A. and Misra, H. S., RecBC enzyme overproduction affects UV and gamma radiation survival of Deinococcus radiodurans. DNA Repair (Amst.), 2008, 7, 40-47.
35. Misra, H. S., Khairnar, N. P., Kota, S., Shrivastava, S., Joshi, V. P. and Apte, S. K., An exonuclease I sensitive DNA repair pathway in Deinococcus radiodurans: a major determinant of radiation resistance. Mol. Microbiol., 2006, 59, 1308-1316.
36. Slade, D., Lindner, A. B., Paul, G. and Radman, M., Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell, 2009, 136, 1044-1055.
37. Bentchikou, E., Servant, P., Coste, G. and Sommer, S., A major role of the RecFOR pathway in DNA double-strand-break repair through ESDSA in Deinococcus radiodurans. PLoS Genet., 2010, 15, e1000774.
38. Narumi, I. et al., The LexA protein from Deinococcus radiodurans is not involved in RecA induction following gamma irradiation. J. Bacteriol., 2001, 183, 6951-6956.
39. Sheng, D., Zheng, Z., Tian, B., Shen, B. and Hua, Y., LexA analog (dra0074) is a regulatory protein that is irrelevant to recA induction. J. Biochem., 2004, 136, 787-793.
40. Kim, J. I. and Cox, M. M., The RecA proteins of Deinococcus radiodurans and Escherichia coli promote DNA strand exchange via inverse pathways. Proc. Natl. Acad. Sci. USA, 2002, 99, 7917-7921.
41. Hua, X. et al., Both OB folds of single-stranded DNA-binding protein are essential for its ssDNA binding activity in Deinococcus radiodurans. Protein Pept. Lett., 2010, 17, 1189-1197.
42. Zahradka, K. et al., Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature, 2006, 443, 569-573.
43. Aravind, L. and Koonin, E. V., DNA-binding proteins and evolution of transcription regulation in the archaea. Nucleic Acids Res., 1999, 27, 4658-4670.
44. Cao, Z., Mueller, C. W. and Julin, D. A., Analysis of the recJ gene and protein from Deinococcus radiodurans. DNA Repair (Amst.), 2010, 9, 66-75.
45. Blasius, M., Shevelev, I. Jolivet, E., Sommer, S. and Hubscher, U., DNA polymerase X from Deinococcus radiodurans possesses a structure modulated 3′-5′ exonuclease activity involved in radioresistance. Mol. Microbiol., 2006, 60, 165-176.
46. Kota, S., Kumar, C. V. and Misra, H. S., Characterization of an ATP-regulated DNA-processing enzyme and thermotolerant phosphoesterase in the radioresistant bacterium Deinococcus radiodurans. Biochem. J., 2010, 431, 149-157.
47. Blasius, M., Buob, R., Shevelev, I. V. and Hubscher, U., Enzymes involved in DNA ligation and end-healing in the radioresistant bacterium, Deinococcus radiodurans. BMC Mol. Biol., 2007, 8, 69.
48. Ivanova, N. et al., Complete genome sequence of Truepera radiovictrix type strain (RQ-24). Stand. Genomic Sci., 2011, 4, 91-99.
49. Daly, M. J. and Minton, K. W., A model of repair of radiationinduced DNA double-strand breaks in extreme radiophile Deinococcus radiodurans. BioEssays, 1995, 17, 457-464.
50. Gerdes, K., Howard, M. and Szarddenings, F., Pushing and pulling in prokaryotic DNA segregation. Cell, 2010, 121, 927-942.
51. Charaka, V. K. and Misra, H. S., Functional characterization of the role of the chromosome I partitioning system in genome segregation in Deinococcus radiodurans. J. Bacteriol., 2012, 194, 5739-5748.
52. Harris, D. R., Tanaka, M., Saveliev, S. V., Jolivet, E., Earl, A. M., Cox, M. M. and Battista, J. R., Preserving genome integrity: the DdrA protein of Deinococcus radiodurans R1. PLoS Biol., 2004, 2, e304.
53. Kamble, V. A., Rajpurohit, Y. S., Srivastava, A. K. and Misra, H. S., Increased synthesis of signaling molecules coincides with reversible inhibition of nucleolytic activity during postirradiation recovery of Deinococcus radiodurans. FEMS Microbiol. Lett., 2010, 303, 18-25.
54. Kota, S. and Misra, H. S., Identification of a DNA processing complex from Deinococcus radiodurans. Biochem. Cell Biol., 2008, 86, 448-458.
55. Das, A. D. and Misra, H. S., DR2417, a hypothetical protein characterized as a novel β-CASP family nuclease in radiation resistant bacterium, Deinococcus radiodurans. Biochim. Biophys. Acta, 2012, 1820, 1052-1061.
56. Liu, Y. et al., Transcriptome dynamics of Deinococcus radiodurans recovering from ionizing radiation. Proc. Natl. Acad. Sci. USA, 2003, 100, 4191-4196.
57. Joshi, B., Schmid, R., Altendorf, K. and Apte, S. K., Protein recycling is a major component of post-irradiation recovery in Deinococcus radiodurans strain R1. Biochem. Biophys. Res. Commun., 2004, 320, 1112-1117.
58. Basu, B. and Apte, S. K., Gamma radiation-induced proteome of Deinococcus radiodurans primarily targets DNA repair and oxidative stress alleviation. Mol. Cell. Proteomics, 2012, 11, M111. 011734.
59. Bonacossa de Almeida, C., Coste, G., Sommer, S. and Bailone, A., Quantification of RecA protein in Deinococcus radiodurans reveals involvement of RecA, but not LexA, in its regulation. Mol. Genet. Genomics, 2002, 268, 28-41.
60. Khan, F., Singh, S. P. and Mishra, B. N., Conservation of the LexA repressor-binding site in Deinococcus radiodurans. J. Integr. Bioinformat., 2008, 24, 5.
61. Earl, A. M., Mohundro, M. M., Mian, I. S. and Battista, J. R., The IrrE protein of Deinococcus radiodurans R1 is a novel regulator of recA expression. J. Bacteriol., 2002, 184, 6216-6224.
62. Chen, H. et al., A novel OxyR sensor and regulator of hydrogen peroxide stress with one cysteine residue in Deinococcus radiodurans. PLOS One 2008, 3, e1602.
63. Yin, L. et al., DRA0336, another OxyR homolog, involved in the antioxidation mechanisms in Deinococcus radiodurans. J. Microbiol., 2010, 48, 473-479.
64. Sheng, D., Li, M., Jiao, J., Sheng, X., Deng, W. and Hua, Y., Repression of recA induction by RecX is independent of the RecA protein in Deinococcus radiodurans. J. Bacteriol., 2010, 192, 3540-3544.
65. Patel, B. A., Moreau, M., Widom, J., Chen, H., Yin, L., Hua, Y. and Crane, B. R., Endogenous nitric oxide regulates the recovery of the radiation-resistant bacterium Deinococcus radiodurans from exposure to UV light. Proc. Natl. Acad. Sci. USA, 2009, 106, 18183-18188.
66. Rajpurohit, Y. S. and Misra, H. S., Characterization of a DNA damage-inducible membrane protein kinase from Deinococcus radiodurans and its role in bacterial radioresistance and DNA strand break repair. Mol. Microbiol., 2010, 77, 1470-1482.
67. Desai, S. S., Rajpurohit, Y. S., Misra, H. S. and Deobagkar, D. N., Characterization of RadS/RadR two-component system role in radiation resistance of Deinococcus radiodurans. Microbiology (SGM), 2011, 157, 2974-2982.
68. Caria, S., de Sanctis, D., Enguita, F. J. and McSweeney, S., Crystallization and preliminary X-ray characterization of a catalytic and ATP-binding domain of a putative PhoR histidine kinase from the gamma-radioresistant bacterium Deinococcus radiodurans. Acta Crystallogr., Sect. F, 2010, 66, 401-404.
69. Rajpurohit, Y. S., Desai, S. S. and Misra, H. S., Pyrroloquinoline quinone and a Ser/Thr quinoprotein kinase support gamma radiation resistance in Deinococcus radiodurans and regulate differential gene expression. J. Basic Microbiol., 2012, doi: 10.1002/ jobm.201100650.
70. Xu, G. et al., DdrB stimulates single-stranded DNA annealing and facilitates RecA-independent DNA repair in Deinococcus radiodurans. DNA Repair (Amst.), 2010, 9, 805-812.
71. Sugiman-Marangos, S. and Junop, M. S., The structure of DdrB from Deinococcus: a new fold for single-stranded DNA binding proteins. Nucleic Acids Res., 2010, 38, 3432-3440.
72. Bouthier, De La Tour, C. et al., The deinococcal DdrB protein is involved in an early step of DNA double strand break repair and in plasmid transformation through its single-strand annealing activity. DNA Repair (Amst.), 2011, 10, 1223-1231.
73. Krisko, A., Smole, Z., Debret, G., Nikolić, N. and Radman, M., Unstructured hydrophilic sequences in prokaryotic proteomes correlate with dehydration tolerance and host association. J. Mol. Biol., 2010, 402, 775-782.
74. Awile, O., Krisko, A., Sbalzarini, I. F. and Zagrovic, B., Intrinsically disordered regions may lower the hydration free energy in proteins: a case study of nudix hydrolase in the bacterium Deinococcus radiodurans. PLoS Comput. Biol., 2010, 15, e1000854.
75. Southworth, M. W. and Perler, F., Protein spilcing of the Deinococcus radiodurans strain R1 Snf2 intein. J. Bacteriol., 2002, 184, 6387-6388.
76. Brace, L. E., Southworth, M. W., Tori, K., Cushing, M. L. and Perler, F., The Deinococcus radiodurans Snf2 intein caught in the act: detection of the class 3 intein signature Block F branched intermediate. Protein Sci., 2010, 19, 1525-1533.
77. Ryzhikov, M., Koroleva, O., Postnov, D., Tran, A. and Korolev, S., Mechanism of RecO recruitment to DNA by single-stranded DNA binding protein. Nucleic Acids Res., 2011, 39, 3509-3614.
78. Das, A. D. and Misra, H. S., Characterization of DRA0282 from Deinococcus radiodurans for its role in bacterial resistance to DNA damage. Microbiology (SGM), 2011, 157, 2196-2205.
79. Daly, M. J. et al., Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science, 2004, 306, 1025-1028.
80. Daly, M. J. et al., Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One, 2010, 5, e12570.
81. Shashidhar, R., Kumar, S. A., Misra, H. S. and Bandekar, J. R., Evaluation of the role of enzymatic and nonenzymatic antioxidant systems in the radiation resistance of Deinococcus. Can. J. Microbiol., 2010, 56, 195-201.
82. Granger, A. C., Gaidamakova, E. K., Matrosova, V. Y., Daly, M. J. and Setlow, P., Effects of Mn and Fe levels on Bacillus subtilis spore resistance and effects of Mn2+, other divalent cations, orthophosphate, and dipicolinic acid on protein resistance to ionizing radiation. Appl. Environ. Microbiol., 2011, 77, 32-40.
83. Kamble, V. A. and Misra, H. S., The SbcCD complex of Deinococcus radiodurans contributes to radioresistance and DNA strand break repair in vivo and exhibits Mre11-Rad50 type activity in vitro. DNA Repair (Amst.), 2010, 9, 488-944.
84. Helmann, J. D., Bacillithiol, a new player in bacterial redox homeostasis. Antioxid. Redox Signal., 2011, 15, 123-133.
85. Misra, H. S., Khairnar, N. P., Atanu, B., Priyadarshini, K. I., Mohan, H. and Apte, S. K., Pyrroloquinoline-quinone: a reactive oxygen species scavenger in bacteria. FEBS Lett., 2004, 578, 26- 30.
86. Rajpurohit, Y. S., Gopalakrishnan, R. and Misra, H. S., Involvement of a protein kinase activity inducer in DNA double strand break repair and radioresistance of Deinococcus radiodurans. J. Bacteriol., 2008, 190, 3948-3954.
87. Wurtmann, E. J. and Wolin, S. L., A role for a bacterial ortholog of the Ro autoantigen in starvation-induced rRNA degradation. Proc. Natl. Acad. Sci. USA, 2010, 107, 4022-4027.
88. Mennecier, S., Servant, P., Coste, G., Bailone, A. and Sommer, S., Mutagenesis via IS transposition in Deinococcus radiodurans. Mol. Microbiol., 2006, 59, 317-325.
89. Pasternak, C., Ton-Hoang, B., Coste, G., Bailone, A., Chandler, M. and Sommer, S., Irradiation-induced Deinococcus radiodurans genome fragmentation triggers transposition of a single resident insertion sequence. PLOS Genet., 2010, 15, e1000799.
90. Hickman, A. B. et al., DNA recognition and the precleavage state during single-stranded DNA transposition in D. radiodurans. EMBO J., 2010, 29, 3840-3852.
91. Gourbeyre, E., Siguier, P. and Chandler, M., Route 66: investigations into the organization and distribution of the IS66 family of prokaryotic insertion sequences. Res. Microbiol., 2010, 161, 136- 143.
92. Repar, J., Cvjetan, S., Slade, D., Radman, M., Zahradka, D. and Zahradka, K., RecA protein assures fidelity of DNA repair and genome stability in Deinococcus radiodurans. DNA Repair (Amst.), 2010, 9, 1151-1161.
93. Zeng, Y. H., Shen, F. T., Tan, C. C., Huang, C. C. and Young, C. C., The flexibility of UV-inducible mutation in Deinococcus ficus as evidenced by the existence of the imuB-dnaE2 gene cassette and generation of superior feather degrading bacteria. Microbiol. Res., 2011, 167, 40-47.
94. Zheng, X., Hu, G. Q., She, Z. S. and Zhu, H., Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes. BMC Genomics, 2011, 12, 361.
95. Krogh, B. O. and Shuman, S., A poxvirus-like type IB topoisomerase family in bacteria. Proc. Natl. Acad. Sci. USA, 2002, 99, 1853-1858.
96. Khairnar, N. P., Misra, H. S. and Apte, S. K., Pyrroloquinolinequinone synthesized in Escherichia coli by pyrroloquinolinequinone synthase of Deinococcus radiodurans plays a role beyond mineral phosphate solubilization. Biochem. Biophys. Res. Commun., 2003, 312, 303-308.
97. Sandigursky, M., Sandigursky, S., Sonati, P., Daly, M. J. and Franklin, W. A., Multiple uracil-DNA glycosylase activities in Deinococcus radiodurans. DNA Repair (Amst.), 2004, 3, 163- 169.
98. Ghosh, S. and Grove, A., The Deinococcus radiodurans-encoded HU protein has two DNA-binding domains. Biochemistry, 2006, 45, 1723-1733.
99. Wu, Y., Chen, W., Zhao, Y., Xu, H. and Hua, Y., Involvement of RecG in H2O2-induced damage repair in Deinococcus radiodurans. Can. J. Microbiol., 2009, 55, 841-848.
100. Kang, C. M., Abbott, D. W., Park, S. T., Dascher, C. C., Cantley, L. C. and Husson, R. N., The Mycobacerium tuberculosis serine/ threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev., 2005, 19, 1692-1704.
101. Prisic, S., Dankwa, S., Schwartz, D., Chou, M. F., Locasale, J. W., Kang, C. M., Bemis, G., Church, G. M., Steen, H. and Husson, R. N., Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Proc. Natl. Acad. Sci. USA, 2010, 107, 7521-7526.
102. Brooks, B. W. and Murray, R. G. E., Nomenclature for Micrococcus radiodurans and other radiation-resistant cocci: Deinococcaceae fam. nov. and Deinococcus gen. nov., including five species. Int. J. Syst. Bacteriol., 1981, 31, 353-360.
103. Eltsov, M. and Dubochet, J., Fine structure of the Deinococcus radiodurans nucleoid revealed by cryoelectron microscopy of vitreous sections. J. Bacteriol., 2005, 187, 8047-8054.
104. Giewekemeyer, K., Thibault, P., Kalbfleisch, S., Beerlink, A., Kewish, C. M., Dierolf, M., Pfeiffer, F. and Salditt, T., Quantitative biological imaging by ptychographic X-ray diffraction microscopy. Proc. Natl. Acad. Sci. USA, 2009, 107, 529-534.