Proteomic and physiological responses of Kineococcus radiotolerans to copper

PLoS ONE

Volumn 5, Issue 8, 2010, Pages

  Bagwell, Christopher E ^a   Hixson, Kim K ^b   Milliken, Charles E ^a   Lopez Ferrer, Daniel ^c   Weitz, Karl K ^c  

^a SAVANNAH RIVER NATIONAL LABORATORY   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; COPPER; SUPEROXIDE DISMUTASE; BACTERIAL PROTEIN;

ACTINOBACTERIA; ANAEROBIC GROWTH; ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BIOACCUMULATION; BIOTECHNOLOGY; CELL FUNCTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CULTURE MEDIUM; DNA REPAIR; ECOSYSTEM RESTORATION; ENZYME REPRESSION; KINEOCOCCUS RADIOTOLERANS; MICROBIAL BIOMASS; NONHUMAN; OPEN READING FRAME; OXIDATIVE STRESS; PHYSIOLOGICAL PROCESS; PROTEIN METABOLISM; PROTEOMICS; ACTINOMYCETALES; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

KINEOCOCCUS RADIOTOLERANS;

ACTINOMYCETALES; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; COPPER; GENE EXPRESSION REGULATION, BACTERIAL; OXIDATIVE STRESS; PROTEOMICS;

EID: 77957870575     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012427     Document Type: Article

References (91)

1. Phillips RW, Wiegel J, Berry CJ, Fliermans C, Peacock AD, et al. (2002) Kineococcus radiotolerans sp. nov., a radiation-resistant, Gram-positive bacterium. Int J Syst Evol Microbiol 52: 933-8.
2. Radajewski S, Duxbury T (2001) Motility responses and desiccation survival of zoospores from the actinomycete Kineosporia sp. strain SR11. Microb Ecol 41: 233-44.
3. Tringe SG, von Mering C, Kobayashi A, Salamov AA, Chen K, et al. (2005) Comparative metagenomics of microbial communities. Science 308: 554-7.
4. Garrity GM, Heimbuch BK, Gagliardi M (1996) Isolation of zoosporogenous actinomycetes from desert soils. Ind Microbiol Biotechnol 17: 268-80.
5. Schabereiter-Gurtner C, Piñar G, Vybiral D, Lubitz W, Rolleke S (2001) Rubrobacter-related bacteria associated with rosy discolouration of masonry and lime wall paintings. Arch Microbiol 176: 347-54.
6. Torre de la JR, Goebel BM, Friedmann EI, Pace NR (2003) Microbial diversity of cryptoendolithic communities from the McMurdo Dry Valleys, Antarctica. Appl Environ Microbiol 69: 3858-67.
7. Kim TK, Garson MJ, Fuerst JA (2005) Marine actinomycetes related to the 'Salinospora' group from the Great Barrier Reef sponge Pseudoceratina clavata. Environ Microbiol 7: 509-518.
8. Mincer TJ, Jensen PR, Kauffman CA, Fenical W (2002) Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 68: 5005-11.
9. Wohl DL, McArthur JV (1998) Actinomycetes-flora associated with submersed freshwater macrophytes. FEMS Microbiol Ecol 26: 135-40.
10. Bagwell CE, Milliken CE, Ghoshroy S, Blom DA (2008) Intracellular copper accumulation enhances the growth of Kineococcus radiotolerans during chronic irradiation. Appl Environ Microbiol 74: 1376-84.
11. Lee SD (2006) Kineococcus marinus sp. nov., isolated from marine sediments of the coast of Jeju, Korea. Int J Syst Evol Microbiol 56: 1279-83.
12. Yokota A, Tamura T, Nishii T, Hasegawa T (1993) Kineococcus aurantiacus gen. nov., sp. nov., a new aerobic, gram-positive, motile coccus with mesodiaminopimelic acid and arabinogalactan in the cell wall. Int J Syst Bacteriol 43: 52-7.
13. O'Halloran TV, Culotta VC (2000) Metallochaperones, an intracellular shuttle service for metal ions. J Biol Chem 275: 25057-60.
14. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV (1999) Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284: 805-8.
15. Lu ZH, Dameron CT, Solioz M (2003) The Enterococcus hirae paradigm of copper homeostasis: Copper chaperone turnover, interactions, and transactions. BioMetals 16: 137-43.
16. Silver S, Phung LT (1996) Bacterial heavy metal resistance: New surprises. Ann Rev Microbiol 50: 753-89.
17. Cooksey DA (1993) Copper uptake and resistance in bacteria. Mol Microbiol 7: 1-5.
18. + extrusion by CopB. Biochem Biophys Res Commun 202: 44-8.
19. Lu ZH, Solioz M (2001) Copper induced proteolysis of the CopZ copper chaperone of Enterococcus hirae. J Biol Chem 276: 47822-27.
20. Cha J, Cooksey DA (1991) Copper resistance in Pseuodomonas syringae mediated by periplasmic and outer membrane proteins. Proc Natl Acad Sci USA 88: 8915-19.
21. Cooksey DA, Azad HR (1992) Accumulation of copper and other metals by copper-resistant plant-pathogenic and saprophytic pseudomonads. Appl Environ Microbiol 58: 274-78.
22. Macomber L, Rensing C, Imlay JA (2007) Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J Bacteriol 189: 1616-26.
23. Coombs JT, Franco CMM (2003) Isolation and identification of actinobacteria from surface-sterilized wheat roots. Appl Environ Microbiol 69: 5603-5608.
24. Gómez-Silva B, Rainey FA, Warren-Rhodes KA, McKay CP, Navarro-González R (2008) Atacama desert soil microbiology. In: Dion P, Nautiyal CS, eds. Microbiology of Extreme Soils, Soil Biology, Vol 13. Springer Berlin Heidelberg. pp 117-132.
25. Kuhlman KR, Fusco WG, La Duc MT, Allenbach LB, Ball CL, et al. (2006) Diversity of microorganisms within rock varnish in the Whipple Mountains, California. Appl Environ Microbiol 72: 1708-15.
26. West TS, Coombs TL (1981) Soil as the source of trace elements. Philosophical Transactions of the Royal Society of London. Series B. Biological Sciences 294: 19-39.
27. Imperi F, Caneva G, Cancellieri L, Ricci MA, Sodo A, et al. (2007) The bacterial aetiology of rosy discoloration of ancient wall paintings. Environ Microbiol 9: 2894-902.
28. Urzí C, Brusetti L, Salamone P, Sorlini C, Stackebrandt E, et al. (2001) Biodiversity of Geodermatophilaceae isolated from altered stones and monuments in the Mediterranean basin. Environ Microbiol 3: 471-79.
29. Urzí C, Salamone P, Schumann P, Stackebrandt E (2000) Marmoricola aurantiacus gen. nov., sp. nov., a coccoid member of the family Nocardioidaceae isolated from a marble statue. Int J Syst Evol Microbiol 50: 529-36.
30. Albarracín VH, Amoroso MJ, Abate CM (2005) Isolation and characterization of indigenous copper-resistant actinomycete strains. Chemie der Erde - Geochemistry 65: 145-56.
31. Fredrickson JK, Zachara JM, Balkwill DL, Kennedy D, Li SMW, et al. (2004) Geomicrobiology of high-level nuclear waste-contaminated vadose sediments at the Hanford site, Washington State. Appl Environ Microbiol 70: 4230-41.
32. Gremion F, Chatzinotas A, Harms H (2003) Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5: 896-907.
33. Haferburg G, Merten D, Büchel G, Kothe E (2007) Biosorption of metal and salt tolerant microbial isolates from a former uranium mining area. Their impact on changes in rare earth element patterns in acid mine drainage. J Bas Microbiol 47: 474-84.
34. Konstantinidis KT, Isaacs N, Fett J, Simpson S, Long DT, et al. (2003) Microbial diversity and resistance to copper in metal-contaminated lake sediment. Microb Ecol 45: 191-202.
35. Schmidt A, Haferburg G, Sineriz M, Merten D, Büchel G, et al. (2005) Heavy metal resistance mechanisms in actinobacteria for survival in AMD contaminated soils. Chemie der Erde - Geochem 65: 131-44.
36. Van Nostrand JD, Khijniak TV, Gentry TJ, Novak MT, Sowder AG, et al. (2007) Isolation and characterization of four Gram-positive nickel-tolerant microorganisms from contaminated sediments. Micro Ecol 53: 670-82.
37. Ishiguro EE, Wolfe RS (1970) Control of morphogenesis in Geodermatophilus: Ultrastructural studies. J Bacteriol 104: 566-80.
38. Luedemann GM (1968) Geodermatophilus, a new genus of the Dermatophilaceae (Actinomycetales). J Bacteriol 96: 1848-58.
39. Williams ST, Sharpe ME, Holt JG (1989) Bergey's manual of systematic bacteriology, Vol 4. Williams & Wilkins. Baltimore, MD, USA.
40. Johnston DW, Cross T (1976) Actinomycetes in lake muds: dormant spores or metabolically active mycelium? Freshwater Biol 6: 465-470.
41. Mayfield CI, Williams ST, Ruddick SM, Hatfield HL (1972) Studies on the ecology of actinomycetes in soil IV. Observations on the form and growth of streptomycetes in soil. Soil Biol Biochem 4: 79-86.
42. Baikun L, Bishop PL (2004) Micro-profiles of activated sludge floc determined using microelectrodes. Water Res 38: 1248-58.
43. Daly MJ, Gaidamakova EK, Matrosova VY, Vasilenko A, Zhai M, et al. (2004) Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance. Science 306: 1025-8.
44. Silva JC, Gorenstein MV, Li GZ, Vissers JP, Geromanos SJ (2006) Absolute quantification of proteins by LCMSE: a virtue of parallel MS acquisition. Mol Cell Proteomics 5: 144-56.
45. Gupta N, Pevzner PA (2009) False discovery of protein identifications: a strike against the two-peptide rule. J Proteome Res 8: 4173-81.
46. Kim S, Gupta N, Pevzner PA (2008) Spectral probabilities and generating functions of tandem mass spectra: a strike against decoy databases. J Proteome Res 7: 3354-63.
47. Bagwell CE, Bhat S, Hawkins GM, Smith BW, Biswas T, et al. (2008) Survival in nuclear waste, extreme resistance, and potential applications gleaned from the genome sequence of Kineococcus radiotolerans SRS30216. PLoS One 3(12): e3878.
48. Ellington MJK, Sawers G, Sears HJ, Spiro S, Richardson DJ, et al. (2003) Characterization of the expression and activity of the periplasmic nitrate reductase of Paracoccus pantotrophus in chemostat cultures. Microbiol 149: 1533-40.
49. Ansaldi M, Théraulaz L, Baraquet C, Panis G, Méjean V (2007) Aerobic TMAO respiration in Escherichia coli. Mol Microbiol 66: 484-94.
50. Deaconescu AM, Savery N, Darst SA (2007) The bacterial transcription-repair coupling factor. Curr Opin Struct Biol 17: 96-102.
51. Qing Z, Xinjue Z, Hong XU, Bujin XU, Yuejin H (2006) RadA: A protein involved in DNA damage repair processes of Deinococcus radiodurans R1. Chinese Sci Bull 51: 2993-9.
52. Song Y, Sargentini NJ (1996) Escherichia coli DNA repair genes radA and sms are the same gene. J Bacteriol 178: 5045-8.
53. Su M, Cavallo S, Stefanini S, Chiancone E, Chasteen ND (2005) The so-called Listeria innocua ferritin is a Dps protein. Iron incorporation, detoxification, and DNA protection properties. Biochem 44: 5572-78.
54. Dameron CT, Harrison MD (1998) Mechanisms for protection against copper toxicity. Am J Clin Nutr 67: 1091S-7S.
55. Denisov ET, Afanas'ev IB (2005) DNA oxidative damage. In: Denisov ET, Afanas'ev IB, eds. Oxidation and Antioxidants in Organic Chemistry and Biology. CRC Press, Taylor & Francis Group. pp 819-30.
56. Erardi FX, Failla ML, Falkinham JO (1987) Plasmid-encoded copper resistance and precipitation by Mycobacterium scrofulaceum. Appl Environ Microbiol 53: 1951-54.
57. Fabisiak JP, Tyurin VA, Tyurina YY, Borisenko GG, Korotaeva A, et al. (1999) Redox regulation of copper-metallothionein. Arch Biochem Biophy 363: 171-81.
58. Keyer K, Imlay JA (1996) Superoxide accelerates DNA damage by elevating free-iron levels. Proc Natl Acad Sci USA 93: 13635-40.
59. Hassan HM, Fridovich I (1977) Regulation of the synthesis of superoxide dismutase in Escherichia coli. J Biol Chem 252: 7667-72.
60. Culotta VC, Joh HD, Lin SJ, Slekar KH, Strain J (1995) A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. J Biol Chem 270: 29991-7.
61. Geslin C, Llanos J, Prieur D, Jeanthon C (2001) The manganese and iron superoxide dismutases protect Escherichia coli from heavy metal toxicity. Res Microbiol 152: 901-5.
62. Fridovich I (1983) Superoxide radical: an endogenous toxicant. Ann Rev Pharmacol Toxicol 23: 239-57.
63. Scott MD, Meshnick SR, Eaton JW (1987) Superoxide dismutase-rich bacteria. J Biol Chem 262: 3640-5.
64. Schwartz CE, Krall J, Norton L, McKay K, Kay D, et al. (1983) Catalase and superoxide dismutase in Escheriichia coli. J Biol Chem 258: 6277-81.
65. Loewen PC (1984) Isolation of catalase-deficient Escherichia coli mutants and genetic mapping of katE, a locus that affects catalase activity. J Bacteriol 157: 622-6.
66. Hassan HM, Fridovich I (1979) Intracellular production of superoxide radical and hydrogen peroxide by redox active compounds. Arch Biochem Biophys 196: 385-95.
67. Kelner MJ, Bagnell R (1990) Alteration of endogenous glutathione peroxidase, manganese superoxide dismutase, and glutathione transferase activity in cells transfected with a copper-zinc superoxide dismutase expression vector. J Biol Chem 265: 10872-5.
68. Rosadini CV, Wong SMS, Akerley BJ (2008) The periplasmic disulfide oxidoreductase DsbA contributes to Haemophilus influenzae pathogenesis. Infect and Immunity 76: 1498-1508.
69. Peek JA, Taylor RK (1992) Characterization of a periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proc Natl Acad Sci USA 89: 6210-14.
70. Bringer MA, Rolhion N, Glasser AL, Darfeuille-Michaud A (2007) The oxidoreductase DsbA plays a key role in the ability of the Crohn's diseaseassociated adherent-invasive Escherichia coli strain LF82 to resist macrophage killing. J Bacteriol 189: 4860-71.
71. Swaving J, De Bont JAM, Westphal A, De Kok A (1996) A novel type pyridine nucleotide-disulfide oxidoreductase is essential for NAD + - and NADPHdependent degradation of epoxyalkanes by Xanthobacter strain Py2. J Bacteriol 178: 6644-6.
72. Attfield PV (1987) Trehalose accumulates in Saccharomyces cerevisiae during exposure to agents that induce heat shock response. FEBS Letters 225: 259-63.
73. De Smet KAL, Weston A, Brown IN, Young DB, Robertson BD (2000) Three pathways for trehalose biosynthesis in mycobacteria. Microbiol 146: 199-208.
74. Monobe M, Uzawa A, Hino M, Ando K, Kojima S (2005) Glycine betaine, a beer component, protects radiation-induced injury. J Radiat Res 46: 117-21.
75. Grassmann J, Hippeli S, Elstner EF (2002) Plant's defence and its benefits for animals and medicine: role of phenolics and terpenoids in avoiding oxygen stress. Plant Physiol Biochem 40: 471-8.
76. De Mot R, Nagy I, Walz J, Baumeister W (1999) Proteasomes and other selfcompartmentalizing proteases in prokaryotes. Trends in Microbiol 7: 88-92.
77. Liu M, Peng F, Wang Y, Zhang K, Chen G, et al. (2009) Kineococcus xinjiangensis sp. nov., isolated from desert sand. Int J Syst Evol Microbiol 59: 1090-3.
78. Han WD, Kawamoto S, Hosoya Y, Fujita M, Sadaie Y, et al. (1998) A novel sporulation-control gene (spoOM) of Bacillus subtilis with a sigma-H-regulated promoter. Gene 217: 31-40.
79. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176: 269-75.
80. Achard-Joris M, Moreau JL, Lucas M, Baudrimont M, Mesmer-Dudons N, et al. (2007) Role of metallothioneins in superoxide radical generation during copper redox cycling: Defining the fundamental function of metallothioneins. Biochimie 89: 1474-88.
81. Kodali VP, Sen R (2008) Antioxidant and free radical scavenging activities of an exopolysaccharide from a probiotic bacterium. Biotechnol J 3: 245-51.
82. Milagres AMF, Muchuca A, Napoleão D (1999) Detection of siderophore production from several fungi and bacteria by a modification of chrome azurol S (CAS) agar plate assay. J Microbiol Methods 37: 1-6.
83. Makarova KS, Omelchenko MV, Gaidamokova EK, Matrosova VY, Vasilenko A, et al. (2007) Deinococcus geothermalis: The pool of extreme radiation resistance genes shrinks. PLoS ONE 2(9): e955.
84. Masselon C, Pasa-Tolic L, Tolic N, Anderson GA, Bogdanov B, et al. (2005) Targeted comparative proteomics by liquid chromatography-tandem fourier ion cyclotron resonance mass spectrometry. Anal Chem 77: 400-6.
85. Qian WJ, Liu T, Monroe ME, Strittmatter EF, Jacobs JM, et al. (2005) Probability-based evaluation of peptide and protein identifications from tandem mass spectrometry and SEQUEST analysis: The human proteome. J Proteome Res 4: 53-62.
86. Shen Y, Tolic N, Zhao R, Pasa-Tolic L, Li L, et al. (2001) High-throughput proteomics using high-efficiency multiple-capillary liquid chromatography with on-line high-performance ESI FTICR mass spectrometry. Anal Chem 73: 3011-21.
87. Smith RD, Anderson GA, Lipton MS, Pasa-Tolic L, Shen Y, et al. (2002) An accurate mass tag strategy for quantitative and high-throughput proteome measurements. Proteomics 2: 513-23.
88. Eng JK, McCormack AL, Yates JR (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 5: 976-989.
89. Lopez-Ferrer D, Martinez-Bartolome S, Villar M, Campillos M, Martin- Maroto F, et al. (2004) Statistical model for large-scale peptide identification in databases from tandem mass spectra using SEQUEST. Anal Chem 76: 6853-60.
90. Zimmer JS, Monroe ME, Qian WJ, Smith RD (2006) Advances in proteomics data analysis and display using an accurate mass and time tag approach. Mass Spectrom Rev 25: 450-482.
91. Polpitiya AD, Qian WJ, Jaitly N, Petyuk VA, Adkins JN, et al. (2008) DAnTE: a statistical tool for quantitative analysis of -omics data. Bioinformatics 24: 1556-87.