Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Genome-Wide Response of Deinococcus radiodurans on Cadmium Toxicity

  • Joe, Min-Ho (Radiation Research Division for Biotechnology, Korea Atomic Energy Research Institute) ;
  • Jung, Sun-Wook (Radiation Research Division for Biotechnology, Korea Atomic Energy Research Institute) ;
  • Im, Seong-Hun (Radiation Research Division for Biotechnology, Korea Atomic Energy Research Institute) ;
  • Lim, Sang-Yong (Radiation Research Division for Biotechnology, Korea Atomic Energy Research Institute) ;
  • Song, Hyun-Pa (Radiation Research Division for Biotechnology, Korea Atomic Energy Research Institute) ;
  • Kwon, Oh-Suk (Integrative Omics Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Kim, Dong-Ho (Radiation Research Division for Biotechnology, Korea Atomic Energy Research Institute)
  • Received : 2010.12.16
  • Accepted : 2011.01.29
  • Published : 2011.04.28
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Abstract

Deinococcus radiodurans is extremely resistant to various genotoxic conditions and chemicals. In this study, we characterized the effect of a sublethal concentration (100 ${\mu}M$) of cadmium (Cd) on D. radiodurans using a whole-genome DNA microarray. Time-course global gene expression profiling showed that 1,505 genes out of 3,116 total ORFs were differentially expressed more than 2-fold in response to Cd treatment for at least one timepoint. The majority of the upregulated genes are related to iron uptake, cysteine biosynthesis, protein disulfide stress, and various types of DNA repair systems. The enhanced upregulation of genes involved in cysteine biosynthesis and disulfide stress indicate that Cd has a high affinity for sulfur compounds. Provocation of iron deficiency and growth resumption of Cd-treated cells by iron supplementation also indicates that CdS forms in iron-sulfur-containing proteins such as the [Fe-S] cluster. Induction of base excision, mismatch, and recombinational repair systems indicates that various types of DNA damage, especially base excision, were enhanced by Cd. Exposure to sublethal Cd stress reduces the growth rate, and many of the downregulated genes are related to cell growth, including biosynthesis of cell membrane, translation, and transcription. The differential expression of 52 regulatory genes suggests a dynamic operation of complex regulatory networks by Cd-induced stress. These results demonstrate the effect of Cd exposure on D. radiodurans and how the related genes are expressed by this stress.

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References

  1. Ackerley, D. F., C. F. Gonzalez, M. Keyhan, R. Blake 2 nd , and A. Matin. 2004. Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. Environ. Microbiol. 6: 851-860. https://doi.org/10.1111/j.1462-2920.2004.00639.x
  2. Beinert, H., R. H. Holm, and E. Münck. 1997. Iron-sulfur clusters: Nature's modular, multipurpose structures. Science 277: 653-659. https://doi.org/10.1126/science.277.5326.653
  3. Beyersmann, D. and S. Hechtenberg. 1997. Cadmium, gene regulation, and cellular signaling in mammalian cells. Toxicol. Appl. Pharmacol. 144: 247-261. https://doi.org/10.1006/taap.1997.8125
  4. Blom, A., W. Harder, and A. Matin. 1992. Unique and overlapping pollutant stress proteins of Escherichia coli. Appl. Environ. Microbiol. 58: 331-334.
  5. Boschi-Muller, S., A. Olry, M. Antoine, and G. Branlant. 2005. The enzymology and biochemistry of methionine sulfoxide reductases. Biochim. Biophys. Acta 1703: 231-238. https://doi.org/10.1016/j.bbapap.2004.09.016
  6. Bulteau, A. L., L. I. Szweda, and B. Friguet. 2006. Mitochondrial protein oxidation and degradation in response to oxidative stress and aging. Exp. Gerontol. 41: 653-657. https://doi.org/10.1016/j.exger.2006.03.013
  7. Busenlehner, L. S., M. A. Pennela, and D. P. Giedroc. 2003. The SmtB/ArsR family of metalloregulatory transcriptional repressors: Structural insights into prokaryotic metal resistance. FEMS Microbiol. Rev. 27: 131-143. https://doi.org/10.1016/S0168-6445(03)00054-8
  8. Cox, M. M. and J. R. Battista. 2005. Deinococcus radiodurans - the consummate survivor. Nat. Rev. Microbiol. 3: 882-892. https://doi.org/10.1038/nrmicro1264
  9. Fahey, R. C. and A. R. Sundquist. 1991. Evolution of glutathione metabolism. Adv. Enzymol. 64: 1-53.
  10. Ferianc, P., A. Farewell, and T. Nystrom. 1998. The cadmiumstress stimulon of Escherichia coli K-12. Microbiology 144: 1045-1050. https://doi.org/10.1099/00221287-144-4-1045
  11. Foloppe, N. and L. Nilsson. 2004. The glutaredoxin -C-P-Y-Cmotif: Influence of peripheral residues. Structure 12: 289-300.
  12. Giaginis, C., E. Gatzidou, and S. Theocharis. 2006. DNA repair systems as targets of cadmium toxicity. Toxicol. Appl. Pharmacol. 213: 282-290. https://doi.org/10.1016/j.taap.2006.03.008
  13. Gomes, D. S., M. D. Pereira, A. D. Panek, L. R. Andrade, and E. C. Eleutherio. 2008. Apoptosis as a mechanism for removal of mutated cells of Saccharomyces cerevisiae: The role of Grx2 under cadmium exposure. Biochim. Biophys. Acta 1780: 160-166. https://doi.org/10.1016/j.bbagen.2007.09.014
  14. Gottesman, S. 2003. Proteolysis in bacterial regulatory circuits. Annu. Rev. Cell Dev. Biol. 19: 565-587. https://doi.org/10.1146/annurev.cellbio.19.110701.153228
  15. Hanson, P. I. and S. W. Whieheart. 2005. AAA+ proteins: Have engine, will work. Nat. Rev. Mol. Cell Biol. 6: 519-529.
  16. Helbig, K., C. Grosse, and D. H. Nies. 2008. Cadmium toxicity in glutathione mutants of Escherichia coli. J. Bacteriol. 190: 5439-5454. https://doi.org/10.1128/JB.00272-08
  17. Hochgrafe, F., J. Mostertz, D. Pöther, D. Becher, J. D. Helmann, and M. Hecker. 2007. S-Cysteinylation is a general mechanism for thiol protection of Bacillus subtilis proteins after oxidative stress. J. Biol. Chem. 282: 25981-25985. https://doi.org/10.1074/jbc.C700105200
  18. International Agency for Research on Cancer (IARC). 1993. IARC monographs on the evaluation of carcinogenic risks on humans: Beryllium, cadmium, mercury, and exposures in the glass manufacturing industry, pp. 119-238. Lyon, France.
  19. Jin, Y. H., A. B. Clark, R. J. Slebos, H. Al-Refai, J. A. Taylor, T. A. Kunkel, M. A. Resnick, and D. A. Gordenin. 2003. Cadmium is a mutagen that acts by inhibiting mismatch repair. Nat. Genet. 34: 326-329. https://doi.org/10.1038/ng1172
  20. Joe, M. H., S. Y. Lim, S. W. Jung, Y. J. Choi, B. Y. Lee, D. S. Song, J. W. Jung, S. H. Chae, and D. H. Kim. 2008. DNA microarray fabrication of Deinococcus radiodurans R1 for a global gene expression profiling. J. Radiat. Ind. 2: 53-58.
  21. Leichert, L. I., C. Scharf, and M. Hecker. 2003. Global characterization of disulfide stress in Bacillus subtilis. J. Bacteriol. 185: 1967-1975. https://doi.org/10.1128/JB.185.6.1967-1975.2003
  22. Livak, K. and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2_T^{-AAC}$ method. Methods 25: 402-408. https://doi.org/10.1006/meth.2001.1262
  23. Malik, M., J. Capecci, and K. Drlica. 2009. Lon protease is essential for paradoxical survival of Escherichia coli exposed to high concentrations of quinolone. Antimicrob. Agents Chemother. 53: 3103-3105. https://doi.org/10.1128/AAC.00019-09
  24. Michaels, M. L. and J. H. Miller. 1992. The GO system protects organisms from the mutagenic effect of the spontaneous lesion 8-hydroxyguanine (7,8-dihydro-8-oxoguanine). J. Bacteriol. 174: 6321-6325.
  25. Mitra, R. S. 1984. Protein synthesis in Escherichia coli during recovery from exposure to low levels of $Cd^{2+}$. Appl. Environ. Microbiol. 47: 1012-1016.
  26. Mitra, R. S. and I. A. Bernstein. 1978. Single-strand breakage in DNA of Escherichia coli exposed to $Cd^{2+}$. J. Bacteriol. 133: 75-80.
  27. Mogk, A., R. Schmidt, and B. Bukau. 2007. The N-end rule pathway for regulated proteolysis: Prokaryotic and eukaryotic strategies. Trends Cell Biol. 17: 165-172. https://doi.org/10.1016/j.tcb.2007.02.001
  28. Momose, Y. and H. Iwahashi. 2001. Bioassay of cadmium using a DNA microarray: Genome-wide expression patterns of Saccharomyces cerevisiae response to cadmium. Environ. Toxicol. Chem. 20: 2353-2360.
  29. Nies, D. H. 1999. Microbial heavy-metal resistance. Appl. Microbiol. Biotechnol. 51: 730-750. https://doi.org/10.1007/s002530051457
  30. Newton, G. L., K. Arnold, M. S. Price, C. Sherrill, S. B. Delcardayre, Y. Aharonowitz, et al. 1996. Distribution of thiols in microorganisms: Mycothiol is a major thiol in most actinomycetes. J. Bacteriol. 178: 1990-1995.
  31. Newton, G. L., M. Rawat, J. J. La Clair, V. K. Jothivasan, T. Budiarto, C. J. Hamilton, A. Claiborne, J. D. Helmann, and R. C. Fahey. 2009. Bacillithiol is an antioxidant thiol produced in bacilli. Nat. Chem. Biol. 5: 625-627. https://doi.org/10.1038/nchembio.189
  32. Nokhbeh, M. R., S. Boroumandi, N. Pokorny, P. Koziarz, E. S. Paterson, and I. B. Lambert. 2002. Identification and characterization of SnrA, an inducible oxygen-insensitive nitroreductase in Salmonella enterica serovar Typhimurium TA1535. Mutat. Res. 508: 59-70. https://doi.org/10.1016/S0027-5107(02)00174-4
  33. Quackenbush, J. 2002. Microarray data normalization and transformation. Nat. Genet. 32: 496-501. https://doi.org/10.1038/ng1032
  34. Rosen, B. P. 2002. Transport and detoxification systems for transition metals, heavy metals and methalloids in eukaryotic and prokaryotic microbes. Compar. Biochem. Physiol. Part A 133: 689-693. https://doi.org/10.1016/S1095-6433(02)00201-5
  35. Ruotolo, R., G. Marchini, and S. Ottonello. 2008. Membrane transporters and protein traffic networks differentially affecting metal tolerance: A genomic phenotyping study in yeast. Genome Biol. 9: R67.
  36. Slade, D., A. B. Lindner, G. Paul, and M. Radman. 2009. Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 136: 1044-1055. https://doi.org/10.1016/j.cell.2009.01.018
  37. Stohs, S. J. and D. Bagchi. 1995. Oxidative mechanisms in the toxicity of metal ions. Free Radic. Biol. Med. 18: 321-336. https://doi.org/10.1016/0891-5849(94)00159-H
  38. Tanaka, M., A. M. Earl, H. A. Howell, M. J. Park, J. A. Eisen, S. N. Peterson, and J. R. Battista. 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. https://doi.org/10.1534/genetics.104.029249
  39. Thorsen, M., G. G. Perrone, E. Kristiansson, M. Traini, T. Ye, I. W. Dawes, O. Nerman, and M. J. Tamas. 2009. Genetic basis of arsenite and cadmium tolerance in Saccharomyces cerevisiae. BMC Genomics 10: 105. https://doi.org/10.1186/1471-2164-10-105
  40. Tsilibaris, V., G. Maenhaut-Michel, and L. Van Melderen. 2006. Biological roles of the Lon ATP-dependent protease. Res. Microbiol. 157: 701-713. https://doi.org/10.1016/j.resmic.2006.05.004
  41. VanBogelen, R. A., P. M. Kelley, and F. C. Neidhardt. 1987. Differential induction of heat shock, SOS, and oxidation stress regulons and accumulation of nucleotides in Escherichia coli. J. Bacteriol. 169: 26-32.
  42. Wang, A. and D. E. Crowley. 2005. Global gene expression responses to cadmium toxicity in Escherichia coli. J. Bacteriol. 187: 3259-3266. https://doi.org/10.1128/JB.187.9.3259-3266.2005
  43. Wang, L., G. Xu, H. Chen, Y. Zhao, N. Xu, B. Tian, and Y. Hua. 2008. DrRRA: A novel response regulator essential for the extreme radioresistance of Deinococcus radiodurans. Mol. Microbiol. 67: 1211-1222. https://doi.org/10.1111/j.1365-2958.2008.06113.x
  44. Woodbury, R. L., T. Luo, L. Grant, and W. G. Haldenwang. 2004. Mutational analysis of RsbT, an activator of the Bacillus subtilis stress response transcription factor, $\sigma^B$. J. Bacteriol. 186: 2789-2797. https://doi.org/10.1128/JB.186.9.2789-2797.2004
  45. Wu, Y., W. Chen, Y. Zhao, H. Xu, and Y. Hua. 2009. Involvement of RecG in $H_2O_2$-induced damage repair in Deinococcus radiodurans. Can. J. Microbiol. 55: 841-848. https://doi.org/10.1139/W09-028
  46. Yoshihara, T., H. Hodoshima, Y. Miyano, K. Shoji, H. Shimada, and F. Goto. 2006. Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Rep. 25: 365-373. https://doi.org/10.1007/s00299-005-0092-3

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