Extremophiles

, Volume 17, Issue 3, pp 485–497

Effects of intracellular Mn on the radiation resistance of the halophilic archaeon Halobacterium salinarum

  • Kimberly M. Webb
  • Jerry Yu
  • Courtney K. Robinson
  • Tomiya Noboru
  • Yuan C. Lee
  • Jocelyne DiRuggiero
Original Paper

Abstract

Ionizing radiation (IR) is of particular interest in biology because its exposure results in severe oxidative stress to the cell’s macromolecules. Our recent work with extremophiles supports the idea that IR resistance is most likely achieved by a metabolic route, effected by manganese (Mn) antioxidants. Biochemical analysis of “super-IR resistant” mutants of H. salinarum, evolved over multiple cycles of exposure to high doses of IR, confirmed the key role for Mn antioxidants in the IR resistance of this organism. Analysis of the proteome of H. salinarum “super-IR resistant” mutants revealed increased expression for proteins involved in energy metabolism, replenishing the cell with reducing equivalents depleted by the oxidative stress inflicted by IR. Maintenance of redox homeostasis was also activated by the over-expression of coenzyme biosynthesis pathways involved in redox reactions. We propose that in H. salinarum, increased tolerance to IR is a combination of metabolic regulatory adjustments and the accumulation of Mn-antioxidant complexes.

Keywords

Halophiles Mn2+ Oxidative stress Ionizing radiation Proteomics 

Supplementary material

792_2013_533_MOESM1_ESM.docx (427 kb)
Supplementary material 1 (DOCX 478 kb)
792_2013_533_MOESM2_ESM.pdf (65 kb)
Supplementary material 2 (PDF 64 kb)
792_2013_533_MOESM3_ESM.pdf (182 kb)
Supplementary material 3 (PDF 182 kb)

References

  1. Al-Maghrebi M, Fridovich I, Benov L (2002) Manganese supplementation relieves the phenotypic deficits seen in superoxide-dismutase-null Escherichia coli. Arch Biochem Biophys 402:104–109PubMedCrossRefGoogle Scholar
  2. Archibald FS, Fridovich I (1982) Investigations of the state of the manganese in Lactobacillus plantarum. Arch Biochem Biophys 215:589–596PubMedCrossRefGoogle Scholar
  3. Baliga NS, Bjork SJ, Bonneau R, Pan M, Iloanusi C, Kottemann MC, Hood L, DiRuggiero J (2004) Systems level insights into the stress response to UV radiation in the halophilic archaeon Halobacterium NRC-1. Genome Res 14:1025–1035PubMedCrossRefGoogle Scholar
  4. Barnese K, Gralla EB, Cabelli DE, Valentine JS (2008) Manganous phosphate acts as a superoxide dismutase. J Am Chem Soc 130:4604–4606PubMedCrossRefGoogle Scholar
  5. Billi D, Friedmann EI, Hofer KG, Grilli Caiola M, Ocampo-Friedmann R (2000) Ionizing-radiation resistance in the desiccation-tolerant cyanobacterium Chroococcidiopsis. Appl Environ Microbiol 66:1489–1492PubMedCrossRefGoogle Scholar
  6. Bonneau R, Facciotti MT, Reiss DJ, Schmid AK, Pan M, Kaur A, Thorsson V, Shannon P, Johnson MH, Bare JC, Longabaugh W, Vuthoori M, Whitehead K, Madar A, Suzuki L, Mori T, Chang DE, Diruggiero J, Johnson CH, Hood L, Baliga NS (2007) A predictive model for transcriptional control of physiology in a free living cell. Cell 131:1354–1365PubMedCrossRefGoogle Scholar
  7. Celis RT (1990) Mutant of Escherichia coli K-12 with defective phosphorylation of two periplasmic transport proteins. J Biol Chem 265:1787–1793PubMedGoogle Scholar
  8. Chang EC, Kosman DJ (1989) Intracellular Mn(II)-associated superoxide scavenging activity protects Cu, Zn superoxide dismutase-deficient Saccharomyces cerevisiae against dioxygen stress. J Biol Chem 264:12172–12178PubMedGoogle Scholar
  9. Chu LJ, Chen MC, Setter J, Tsai YS, Yang H, Fang X, Ting YS, Shaffer SA, Taylor GK, von Haller PD, Goodlett DR, Ng WV (2011) New structural proteins of Halobacterium salinarum gas vesicle revealed by comparative proteomics analysis. J Proteome Res 10:1170PubMedCrossRefGoogle Scholar
  10. Confalonieri F, Sommer S (2011) Bacterial and archaeal resistance to ionizing radiation. J Phys Conf Series 261. doi:10.1088/1742-6596/1261/1081/012005
  11. Daly MJ (2009) A new perspective on radiation resistance based on Deinococcus radiodurans. Nat Rev Microbiol 7:237–245PubMedCrossRefGoogle Scholar
  12. Daly MJ (2012) Death by protein damage in irradiated cells. DNA Repair 11:12–21PubMedCrossRefGoogle Scholar
  13. Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, Leapman RD, Lai B, Ravel B, Li SM, Kemner KM, Fredrickson JK (2007) Protein oxidation implicated as the primary determinant of bacterial radioresistance. PLoS Biol 5:e92PubMedCrossRefGoogle Scholar
  14. Daly MJ, Gaidamakova EK, Matrosova VY, Kiang JA, Fukumoto R, Lee D-Y, Wehr NB, Viteri GA, Berlett BS, Levine RL (2010) Small-molecule antioxidant proteome-shields in Deinococcus radiodurans. PLoS One 5:e12570PubMedCrossRefGoogle Scholar
  15. DasSarma S, Arora P (2001) Halophiles. In: Encyclopedia of life sciences, Nature Publishing Group, pp 1–9Google Scholar
  16. Davies R, Sinskey AJ (1973) Radiation-resistant mutants of Salmonella typhimurium LT2: development and characterization. J Bacteriol 113:133–144PubMedGoogle Scholar
  17. DeVeaux LC, ller JA, Smith J, Petrisko J, Wells DP, DasSarma S (2007) Extremely radiation-resistant mutants of a halophilic archaeon with increased single-stranded DNA-binding protein (RPA) gene expression. Radiation Res 168:507–514PubMedCrossRefGoogle Scholar
  18. Du J, Gebicki JM (2004) Proteins are major initial cell targets of hydroxyl free radicals. Int J Biochem Cell Biol 36:2334–2343PubMedCrossRefGoogle Scholar
  19. Fredrickson JK, Li SM, Gaidamakova EK, Matrosova VY, Zhai M, Sulloway HM, Scholten JC, Brown MG, Balkwill DL, Daly MJ (2008) Protein oxidation: key to bacterial desiccation resistance? ISME J 2:393–403PubMedCrossRefGoogle Scholar
  20. Goo YA, Yi EC, Baliga NS, Tao WA, Pan M, Aebersold R, Goodlett DR, Hood L, Ng WV (2003) Proteomic analysis of an extreme halophilic archaeon, Halobacterium sp. NRC-1. Mol Cell Proteomics 2(8):506–524PubMedGoogle Scholar
  21. Granger AC, Gaidamakova EK, Matrosova VY, Daly MJ, Setlow P (2011) 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 77:32–40PubMedCrossRefGoogle Scholar
  22. Harris DR, Pollock SV, Wood EA, Goiffon RJ, Klingele AJ, Cabot EL, Schackwitz W, Martin J, Eggington J, Durfee TJ, Middle CM, Norton JE, Popelars MC, Li H, Klugman SA, Hamilton LL, Bane LB, Pennacchio LA, Albert TJ, Perna NT, Cox MM, Battista JR (2009) Directed evolution of ionizing radiation resistance in Escherichia coli. J Bacteriol 191:5240–5252PubMedCrossRefGoogle Scholar
  23. Horsburgh MJ, Wharton SJ, Karavolos M, Foster SJ (2002) Manganese: elemental defence for a life with oxygen. Trends Microbiol 10:496–501PubMedCrossRefGoogle Scholar
  24. Imlay JA (2003) Pathways of oxidative damage. Annu Rev Microbiol 57:395–418PubMedCrossRefGoogle Scholar
  25. Imlay JA (2006) Iron-sulphur clusters and the problem with oxygen. Mol Microbiol 59:1073–1082PubMedCrossRefGoogle Scholar
  26. Imlay JA (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77:755–776PubMedCrossRefGoogle Scholar
  27. Kaur A, Pan M, Meislin M, Facciotti MT, El-Gewely R, Baliga NS (2006) A systems view of haloarchaeal strategies to withstand stress from transition metals. Genome Res 16:841–854PubMedCrossRefGoogle Scholar
  28. Kaur A, Van PT, Busch CR, Robinson CK, Pan M, Pang WL, Reiss D, DiRuggiero J, Baliga NS (2010) Coordination of frontline defense mechanisms under severe oxidative stress. Mol Syst Biol 393: doi:10.1038/msb.2010.1050
  29. Kehres DG, Maguire ME (2003) Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria. FEMS Microbiol Rev 27:263–290PubMedCrossRefGoogle Scholar
  30. Kennedy SP, Ng WV, Salzberg SL, Hood L, DasSarma S (2001) Understanding the adaptation of Halobacterium Species NRC-1 to its extreme environment through computational analysis of its genome sequence. Genome Res 11:1641–1650PubMedCrossRefGoogle Scholar
  31. Kish A, DiRuggiero J (2008) Rad50 is not essential for the Mre11-dependent repair of DNA double-strand breaks in Halobacterium sp. strain NRC-1. J Bacteriol 190:5210–5216PubMedCrossRefGoogle Scholar
  32. Kish A, Kirkali G, Robinson C, Rosenblatt R, Jaruga P, Dizdaroglu M, DiRuggiero J (2009) Salt shield: intracellular salts provide cellular protection against ionizing radiation in the halophilic archaeon, Halobacterium salinarum NRC-1. Environ Microbiol 11:1066PubMedCrossRefGoogle Scholar
  33. Kish A, Griffin PL, Rogers KL, Fogel ML, Hemley RJ, Steele A (2012) High-pressure tolerance in Halobacterium salinarum NRC-1 and other non-piezophilic prokaryotes. Extremophiles 16:355–361PubMedCrossRefGoogle Scholar
  34. Kottemann M, Kish A, Iloanusi C, Bjork S, DiRuggiero J (2005) Physiological responses of the halophilic archaeon Halobacterium sp. strain NRC1 to desiccation and gamma irradiation. Extremophiles 9:219–227PubMedCrossRefGoogle Scholar
  35. Markillie LM, Varnum SM, Hradecky P, Wong KK (1999) Targeted mutagenesis by duplication insertion in the radioresistant bacterium Deinococcus radiodurans: radiation sensitivities of catalase (katA) and superoxide dismutase (sodA) mutants. J Bacteriol 181:666–669Google Scholar
  36. McNaughton RL, Reddi AR, Clement MH, Sharma A, Barnese K, Rosenfeld L, Gralla EB, Valentine JS, Culotta VC, Hoffman BM (2010) Probing in vivo Mn2+ speciation and oxidative stress resistance in yeast cells with electron-nuclear double resonance spectroscopy. Proc Natl Acad Sci USA 107:15335–15339PubMedCrossRefGoogle Scholar
  37. Mendis E, Rajapakse N, Kim SK (2005) Antioxidant properties of a radical-scavenging peptide purified from enzymatically prepared fish skin gelatin hydrolysate. J Agric Food Chem 53:581–587PubMedCrossRefGoogle Scholar
  38. Nauser T, Koppenol WH, Gebicki JM (2005) The kinetics of oxidation of GSH by protein radicals. Biochem J 392:693–701PubMedCrossRefGoogle Scholar
  39. Ogunniyi AD, Mahdi LK, Jennings MP, McEwan AG, McDevitt CA, Van der Hoek MB, Bagley CJ, Hoffmann P, Gould KA, Paton JC (2010) Central role of manganese in regulation of stress responses, physiology, and metabolism in Streptococcus pneumoniae. J Bacteriol 192:4489–4497PubMedCrossRefGoogle Scholar
  40. Oren A, Gunde-Cimerman N (2007) Mycosporines and mycosporine-like amino acids: UV protectants or multipurpose secondary metabolites? FEMS Microbiol Lett 269:1–10PubMedCrossRefGoogle Scholar
  41. Peng X, Xiong YL, Kong B (2009) Antioxidant activity of peptide fractions from whey protein hydrolysates as measured by electron spin resonance. Food Chem 113:196–201CrossRefGoogle Scholar
  42. Puri S, Hohle TH, O’Brian MR (2010) Control of bacterial iron homeostasis by manganese. Proc Natl Acad Sci USA 107:10691PubMedCrossRefGoogle Scholar
  43. Reddi AR, Culotta VC (2011) Regulation of manganese antioxidants by nutrient sensing pathways in Saccharomyces cerevisiae. Genetics 189:1261–1270PubMedCrossRefGoogle Scholar
  44. Riley PA (1994) Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int J Radiat Biol 65:27–33PubMedCrossRefGoogle Scholar
  45. Robinson CK, Webb K, Kaur A, Jaruga P, Dizdaroglu M, Baliga NS, Place A, Diruggiero J (2011) A major role for nonenzymatic antioxidant processes in the radioresistance of Halobacterium salinarum. J Bacteriol 193:1653–1662PubMedCrossRefGoogle Scholar
  46. Scott MD, Meshnick SR, Eaton JW (1989) Superoxide dismutase amplifies organismal sensitivity to ionizing radiation. J Biol Chem 264:2498–2501Google Scholar
  47. Sheih IC, Wu TK, Fang TJ (2009) Antioxidant properties of a new antioxidative peptide from algae protein waste hydrolysate in different oxidation systems. Bioresource Technol 100:3419–3425CrossRefGoogle Scholar
  48. Shirkey B, McMaster NJ, Smith SC, Wright DJ, Rodriguez H, Jaruga P, Birincioglu M, Helm RF, Potts M (2003) Genomic DNA of Nostoc commune (Cyanobacteria) becomes covalently modified during long-term (decades) desiccation but is protected from oxidative damage and degradation. Nucleic Acids Res 31:2995–3005PubMedCrossRefGoogle Scholar
  49. Skowyra A, MacNeill SA (2012) Identification of essential and non-essential single-stranded DNA-binding proteins in a model archaeal organism. Nucleic Acids Res 40:1077–1090PubMedCrossRefGoogle Scholar
  50. Slade D, Radman M (2011) Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75:133PubMedCrossRefGoogle Scholar
  51. Slade D, Lindner AB, Paul G, Radman M (2009) Recombination and replication in DNA repair of heavily irradiated Deinococcus radiodurans. Cell 136:1044–1055PubMedCrossRefGoogle Scholar
  52. Sobota JM, Imlay JA (2011) Iron enzyme ribulose-5-phosphate-3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc Natl Acad Sci USA 108:5402–5407PubMedCrossRefGoogle Scholar
  53. Stroud A, Liddell S, Allers T (2012) Genetic and biochemical identification of a novel single-stranded DNA-binding complex in Haloferax volcanii. Frontiers Microbiol 3:224Google Scholar
  54. Van PT, Schmid AK, King NL, Kaur A, Pan M, Whitehead K, Koide T, Facciotti MT, Goo YA, Deutsch EW, Reiss DJ, Mallick P, Baliga NS (2008) Halobacterium salinarum NRC-1 PeptideAtlas: toward strategies for targeted proteomics and improved proteome coverage. J Proteome Res 7:3755–3764PubMedCrossRefGoogle Scholar
  55. Webb KM, DiRuggiero J (2012) Role of Mn2+ and compatible solutes in the radiation resistance of thermophilic bacteria and archaea. Archaea. Article ID 845756. doi:10.1155/2012/845756
  56. Webb KM, DiRuggiero J (2013) Radiation resistance in extremophiles: fending off multiple attacks. In: Seckbach J, Oren A, Stan-Lotter H (eds) Polyextremophiles: life under multiple forms of stress. Series: cellular origin, life in extreme habitats and astrobiology, vol 27. Springer, Dordrecht. doi:10.1007/978-94-007-6488-0_10
  57. Whitehead K, Kish A, Pan M, Kaur A, Reiss DJ, King N, Hohmann L, DiRuggiero J, Baliga NS (2006) An integrated systems approach for understanding cellular responses to gamma radiation. Mol Syst Biol 47. doi:10.1038/msb4100091
  58. Wold MS (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66:61–92PubMedCrossRefGoogle Scholar
  59. Wu HC, Chen HM, Shiau CY (2003) Free amino acids and peptides as related to antioxidant properties in protein hydrolysates of mackerel (Scomber austriasicus). Food Res Intern 36:949–957CrossRefGoogle Scholar
  60. Yakovleva I, Bhagooli R, Takemura A, Hidaka M (2004) Differential susceptibility to oxidative stress of two scleractinian corals: antioxidant functioning of mycosporine-glycine. Comp Biochem Physiol B Biochem Mol Biol 139:721–730PubMedCrossRefGoogle Scholar
  61. Yao AI, Facciotti MT (2011) Regulatory multidimensionality of gas vesicle biogenesis in Halobacterium salinarum NRC-1. Archaea. Article ID 716456Google Scholar

Copyright information

© Springer Japan 2013

Authors and Affiliations

  • Kimberly M. Webb
    • 1
  • Jerry Yu
    • 1
  • Courtney K. Robinson
    • 1
  • Tomiya Noboru
    • 1
  • Yuan C. Lee
    • 1
  • Jocelyne DiRuggiero
    • 1
  1. 1.Department of BiologyJohns Hopkins UniversityBaltimoreUSA

Personalised recommendations