Global proteomic analysis of the chromate response in arthrobacter sp. strain FB24?

Journal of Proteome Research

Volumn 8, Issue 4, 2009, Pages 1704-1716

  Henne, Kristene L ^a   Turse, Joshua E ^c   Nicora, Carrie D ^c   Lipton, Mary S ^c   Tollaksen, Sandra L ^d   Lindberg, Carl ^d   Babnigg, Gyorgy ^d   Giometti, Carol S ^d   Nakatsu, Cindy H ^b   Thompson, Dorothea K ^a   Konopka, Allan E ^a,c  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^d ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

Arthrobacter; Chromium; Liquid chromatography; Mass spectrometry; Metal resistance; Proteomics; Two dimensional gel electrophoresis

Indexed keywords

CHROMIC ACID; CHROMIUM; PROTEOME; SULFATE; SULFUR;

AMINO ACID SYNTHESIS; ANIMAL CELL; ARTHROBACTER; ARTICLE; BACTERIAL STRAIN; BACTERIUM CULTURE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EVALUATION; GROWTH INHIBITION; INTRACELLULAR SPACE; INTRACELLULAR TRANSPORT; LIQUID CHROMATOGRAPHY; NONHUMAN; PHYSIOLOGICAL PROCESS; PHYSIOLOGICAL STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEOMICS; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ARTHROBACTER; BACTERIAL PROTEINS; CHROMATES; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; PROTEOME; TANDEM MASS SPECTROMETRY;

ARTHROBACTER; ARTHROBACTER SP.;

EID: 65249109282     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr800705f     Document Type: Article

References (72)

1. Jones, D.; Keddie, R. M. The Genus Arthrobacter. In The Prokaryotes: An Evolving Electronic Resource for the Microbiological Community, 3rd edition, release 3.0 ed.; Dworkin, M., Ed. Springer- Verlag: New York, 1999.
2. Benyehuda, G.; Coombs, J.; Ward, P. L.; Balkwill, D.; Barkay, T. Metal resistance among aerobic chemoheterotrophic bacteria from the deep terrestrial subsurface. Can. J. Microbiol. 2003, 49 (2), 151-156.
3. Crocker, F. H.; Fredrickson, J. K.; White, D. C.; Ringelberg, D. B.; Balkwill, D. L. Phylogenetic and physiological diversity of Arthro- bacter strains isolated from unconsolidated subsurface sediments. Microbiology 2000, 146 (6), 1295-1310.
4. Fredrickson, J. K.; Zachara, J. M.; Balkwill, D. L.; Kennedy, D.; Li, S. M.; Kostandarithes, H. M.; Daly, M. J.; Romine, M. F.; Brockman, F. J. Geomicrobiology of high-level nuclear waste-contaminated vadose sediments at the Hanford site, Washington state. Appl. Environ. Microbiol. 2004, 70 (7), 4230-4241.
5. Garten, C. T., Jr.; Hamby, D. M.; Schreckhise, R. G. Radiocesium discharges and subsequent environmental transport at the major US weapons production facilities. Sci. Total Environ. 2000, 255 (1-3), 55-73.
6. Kimbrough, D. E.; Cohen, Y.; Winer, A. M.; Creelman, L.; Mabuni, C. A critical assessment of chromium in the environment. Crit. Rev. Environ. Sci. Technol. 1999, 29 (1), 1-46.
7. Ding, M.; Shi, X. Molecular mechanisms of Cr(VI)-induced carcinogenesis. Mol. Cell. Biochem. 2002, 234-235 (1-2), 293-300.
8. Giller, K. E.; Witter, E.; McGrath, S. P. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: A review. Soil Biol. Biochem. 1998, 30 (10-11), 1389-1414.
9. Nakatsu, C. H.; Carmosini, N.; Baldwin, B.; Beasley, F.; Kourtev, P.; Konopka, A. Soil microbial community responses to additions of organic carbon substrates and heavy metals (Pb and Cr). Appl. Environ. Microbiol. 2005, 71 (12), 7679-89.
10. Beasley, F. C. Characterization of Diversity, Chromate Resistance and Aromatic Hydrocarbon Degradation Among Arthrobacter Isolates from Mixed Waste Soil. Masters Thesis, Purdue University, West Lafayette, IN 2004.
11. Camargo, F. A.; Okeke, B. C.; Bento, F. M.; Frankenberger, W. T. Diversity of chromium-resistant bacteria isolated from soils contaminated with dichromate. Appl. Soil Ecol. 2005, 29, 193-202.
12. Cervantes, C.; Silver, S. Plasmid chromate resistance and chromate reduction. Plasmid 1992, 27 (1), 65-71.
13. Juhnke, S.; Peitzsch, N.; Hubener, N.; Grosse, C.; Nies, D. H. New genes involved in chromate resistance in Ralstonia metallidurans strain CH34. Arch. Microbiol. 2002, 179 (1), 15-25.
14. Viti, C.; Pace, A.; Giovannetti, L. Characterization of Cr(VI)-resistant bacteria isolated from chromium-contaminated soil by tannery activity. Curr. Microbiol. 2003, 46 (1), 1-5.
15. Viti, C.; Decorosi, F.; Tatti, E.; Giovannetti, L. Characterization of chromate-resistant and -reducing bacteria by traditional means and by a high-throughput phenomic technique for bioremediation purposes. Biotechnol. Prog. 2007, 23 (3), 553-559.
16. Giometti, C. S.; Reich, C.; Tollaksen, S.; Babnigg, G.; Lim, H.; Zhu, W.; Yates, J.; Olsen, G. Global analysis of a "simple" proteome: Methanococcus jannaschii. J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 2002, 782 (1-2), 227-243.
17. VanBogelen, R. A.; Schiller, E. E.; Thomas, J. D.; Neidhardt, F. C. Diagnosis of cellular states of microbial organisms using proteomics. Electrophoresis 1999, 20 (11), 2149-2159.
18. Evans, C. R.; Jorgenson, J. W. Multidimensional LC-LC and LC- CE for high-resolution separations of biological molecules. Anal. Bioanal. Chem. 2004, 378 (8), 1952-1961.
19. Norbeck, A. D.; Callister, S. J.; Monroe, M. E.; Jaitly, N.; Elias, D. A.; Lipton, M. S.; Smith, R. D. Proteomic approaches to bacterial differentiation. J. Microbiol. Methods 2006, 67 (3), 473-486.
20. Ramagli, L. S. Quantifying protein in 2-D PAGE solubilization buffers. Methods Mol. Biol. 1999, 112, 99-103.
21. Anderson, N. G.; Anderson, N. L. Analytical techniques for cell fractions. XXI. Two-dimensional analysis of serum and tissue proteins: multiple isoelectric focusing. Anal. Biochem. 1978, 85 (2), 331-340.
22. Anderson, N. L.; Anderson, N. G. Analytical techniques for cell fractions. XXII. Two-dimensional analysis of serum and tissue proteins: multiple gradient-slab gel electrophoresis. Anal. Biochem. 1978, 85 (2), 341-354.
23. O'Farrell, P. H. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 1975, 250 (10), 4007-4021.
24. Giometti, C. S.; Gemmell, M. A.; Tollaksen, S. L.; Taylor, J. Quantitation of human leukocyte proteins after silver staining: a studywith two-dimensional electrophoresis. Electrophoresis 1991, 12 (7-8), 536-543.
25. Giometti, C. S.; Tollaksen, S. L.; Gemmell, M. A.; Burcham, J.; Peraino, C. A heritable variant of mouse liver ornithine ami- notransferase (EC 2.6.1.13) induced by ethylnitrosourea. J. Biol. Chem. 1988, 263 (30), 15781-15784.
26. Ahrendt, A. J.; Tollaksen, S. L.; Lindberg, C.; Zhu, W.; Yates, J. R., III; Nevin, K. P.; Babnigg, G.; Lovley, D. R.; Giometti, C. S. Steady state protein levels in Geobacter metallireducens grown with iron (III) citrate or nitrate as terminal electron acceptor. Proteomics 2007, 7 (22), 4148-4157.
27. Lipton, M. S.; Pasa-Tolic, L.; Anderson, G. A.; Anderson, D. J.; Auberry, D. L.; Battista, J. R.; Daly, M. J.; Fredrickson, J.; Hixson, K. K.; Kostandarithes, H.; Masselon, C.; Markillie, L. M.; Moore, R. J.; Romine, M. F.; Shen, Y.; Stritmatter, E.; Tolic, N.; Udseth, H. R.; Venkateswaran, A.; Wong, K.-K.; Zhao, R.; Smith, R. D. From the Cover: Global analysis of the Deinococcus radiodurans pro- teome by using accurate mass tags. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (17), 11049-11054.
28. Smith, R. D.; Anderson, G. A.; Lipton, M. S.; Pasa-Tolic, L.; Shen, Y.; Conrads, T. P.; Veenstra, T. D.; Udseth, H. R. An accurate mass tag strategy for quantitative and high-throughput proteome measurements. Proteomics 2002, 2 (5), 513-523.
29. Lipton, M. S.; Romine, M. F.; Monroe, M. E.; Elias, D. A.; Pasa- Tolic, L.; Anderson, G. A.; Anderson, D. J.; Fredrickson, J.; Hixson, K. K.; Masselon, C.; Mottaz, H.; Tolic, N.; Smith, R. D. AMT tag approach to proteomic characterization of Deinococcus radiodu- rans and Shewanella oneidensis. Methods Biochem. Anal. 2006, 49, 113-134.
30. Eng, J. K.; McCormack, A. L.; Yates, J. R., III. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 1994, 5 (11), 976-989.
31. Washburn, M. P.; Wolters, D.; Yates, J. R., III. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 2001, 19 (3), 242-247.
32. Qian, W. J.; Liu, T.; Monroe, M. E.; Strittmatter, E. F.; Jacobs, J. M.; Kangas, L. J.; Petritis, K.; Camp, D. G., II; Smith, R. D. Probability- based evaluation of peptide and protein identifications from tandem mass spectrometry and SEQUEST analysis: the human proteome. J. Proteome Res. 2005, 4 (1), 53-62.
33. Lu, P.; Vogel, C.; Wang, R.; Yao, X.; Marcotte, E. M. Absolute protein expression profiling estimates the relative contributions of tran- scriptional and translational regulation. Nat. Biotechnol. 2007, 25 (1), 117-124.
34. Wang, H.; Qian, W. J.; Chin, M. H.; Petyuk, V. A.; Barry, R. C.; Liu, T.; Gritsenko, M. A.; Mottaz, H. M.; Moore, R. J.; Camp Ii, D. G.; Khan, A. H.; Smith, D. J.; Smith, R. D. Characterization of the mouse brain proteome using global proteomic analysis complemented with cysteinyl-peptide enrichment. J. Proteome Res. 2006, 5 (2), 361-369.
35. Zhu, W.; Reich, C. I.; Olsen, G. J.; Giometti, C. S.; Yates, J. R., III. Shotgun proteomics of Methanococcus jannaschii and insights into methanogenesis. J. Proteome Res. 2004, 3 (3), 538-548.
36. Ziegler, D. M. Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu. Rev. Biochem. 1985, 54, 305-329.
37. Moran, L. K.; Gutteridge, J. M.; Quinlan, G. J. Thiols in cellular redox signalling and control. Curr. Med. Chem. 2001, 8 (7), 763772.
38. Fucci, L.; Oliver, C. N.; Coon, M. J.; Stadtman, E. R. Inactivation of key metabolic enzymes by mixed-function oxidation reactions: possible implication in protein turnover and ageing. Proc. Natl. Acad. Sci. U.S.A. 1983, 80 (6), 1521-1525.
39. Tamarit, J.; Cabiscol, E.; Ros, J. Identification of the major oxidatively damaged proteins in Escherichia coli cells exposed to oxidative stress. J. Biol. Chem. 1998, 273 (5), 3027-3032.
40. Weber, H.; Engelmann, S.; Becher, D.; Hecker, M. Oxidative stress triggers thiol oxidation in the glyceraldehyde-3-phosphate dehy- drogenase of Staphylococcus aureus. Mol. Microbiol. 2004, 52 (1), 133-140.
41. Kamada, N.; Yasuhara, A.; Takano, Y.; Nakano, T.; Ikeda, M. Effect of transketolase modifications on carbon flow to the purine- nucleotide pathway in Corynebacterium ammoniagenes. Appl. Microbiol. Biotechnol. 2001, 56 (5-6), 710-717.
42. Ohtake, H.; Cervantes, C.; Silver, S. Decreased chromate uptake in Pseudomonas fluorescens carrying a chromate resistance plas- mid. J. Bacteriol. 1987, 169 (8), 3853-3856.
43. Ackerley, D. F.; Barak, Y.; Lynch, S. V.; Curtin, J.; Matin, A. Effect of chromate stress on Escherichia coli K-12. J. Bacteriol. 2006, 188 (9), 3371-3381.
44. Brown, S. D.; Thompson, M. R.; Verberkmoes, N. C.; Chourey, K.; Shah, M.; Zhou, J.; Hettich, R. L.; Thompson, D. K. Molecular dynamics of the Shewanella oneidensis response to chromate stress. Mol. Cell. Proteomics 2006, 5 (6), 1054-1071.
45. Hu, P.; Brodie, E. L.; Suzuki, Y.; McAdams, H. H.; Andersen, G. L. Whole-genome transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J. Bacteriol. 2005, 187 (24), 8437-8449.
46. Thompson, M. R.; Verberkmoes, N. C.; Chourey, K.; Shah, M.; Thompson, D. K.; Hettich, R. L. Dosage-dependent proteome response of Shewanella oneidensis MR-1 to acute chromate challenge. J. Proteome Res. 2007, 6 (5), 1745-1757.
47. Lipton, M. S.; Pasa-Tolic, L.; Anderson, G. A.; Anderson, D. J.; Auberry, D. L.; Battista, J. R.; Daly, M. J.; Fredrickson, J.; Hixson, K. K.; Kostandarithes, H.; Masselon, C.; Markillie, L. M.; Moore, R. J.; Romine, M. F.; Shen, Y.; Stritmatter, E.; Tolic, N.; Udseth, H. R.; Venkateswaran, A.; Wong, K.-K.; Zhao, R.; Smith, R. D. From the Cover: Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags. Proc. Natl. Acad. Sci. U.S.A. 2002, 99 (17), 11049-11054.
48. Carrondo, M. A. Ferritins, iron uptake and storage from the bacterioferritin viewpoint. EMBO J. 2003, 22 (9), 1959-1968.
49. Miranda, A. T.; Gonzalez, M. V.; Gonzalez, G.; Vargas, E.; Campos- Garcia, J.; Cervantes, C. Involvement of DNA helicases in chromate resistance by Pseudomonas aeruginosa PAO1. Mutat. Res. 2005, 578 (1-2), 202-209.
50. Wang, C. C.; Newton, A. Iron transport in Escherichia coli: relationship between chromium sensitivity and high iron requirement in mutants of Escherichia coli. J. Bacteriol. 1969, 98 (3), 1135-1141.
51. Bagchi, D.; Stohs, S. J.; Downs, B. W.; Bagchi, M.; Preuss, H. G. Cytotoxicity and oxidative mechanisms of different forms of chromium. Toxicology 2002, 180 (1), 5-22.
52. van der Ploeg, J. R.; Cummings, N. J.; Leisinger, T.; ConnertonI. F. Bacillus subtilis genes for the utilization of sulfur from aliphatic sulfonates. Microbiology 1998, 144 (9), 2555-2561.
53. van Der Ploeg, J. R.; Iwanicka-Nowicka, R.; Bykowski, T.; Hryniewicz, M. M.; Leisinger, T. The Escherichia coli ssuEADCB gene cluster is required for the utilization of sulfur from aliphatic sulfonates and is regulated by the transcriptional activator Cbl. J. Biol. Chem. 1999, 274 (41), 29358-29365.
54. Sutcliffe, I. C.; Harrington, D. J. Lipoproteins of Mycobacterium tuberculosis: an abundant and functionally diverse class of cell envelope components. FEMS Microbiol. Rev. 2004, 28 (5), 645-659.
55. Borremans, B.; Hobman, J. L.; Provoost, A.; Brown, N. L.; van Der Lelie, D. Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. J. Bacteriol. 2001, 183 (19), 5651-5658.
56. Yamamoto, K.; Ishihama, A. Transcriptional response of Escheri- chia coli to external copper. Mol. Microbiol. 2005, 56 (1), 215-227.
57. Snyder, W. B.; Davis, L. J.; Danese, P. N.; Cosma, C. L.; Silhavy, T. J. Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J. Bacteriol. 1995, 177 (15), 4216-4223.
58. Zheng, J.; He, C.; Singh, V. K.; Martin, N. L.; Jia, Z. Crystal structure of a novel prokaryotic Ser/Thr kinase and its implication in the Cpx stress response pathway. Mol. Microbiol. 2007, 63 (5), 1360-1371.
59. Han, G.; Zhang, C. C. On the origin of Ser/Thr kinases in a prokaryote. FEMS Microbiol. Lett. 2001, 200 (1), 79-84.
60. Joshi, B.; Janda, L.; Stoytcheva, Z.; Tichy, P. PkwA, a WD-repeat protein, is expressed in spore-derived mycelium of Thermomono- spora curvata and phosphorylation of its WD domain could act as a molecular switch. Microbiology 2000, 146 (12), 3259-3267.
61. Neer, E. J.; Schmidt, C. J.; Nambudripad, R.; Smith, T. F. The ancient regulatory-protein family of WD-repeat proteins. Nature 1994, 371 (6495), 297-300.
62. Molenaar, D.; van der Rest, M. E.; Drysch, A.; Yucel, R. Functions of the membrane-associated and cytoplasmic malate dehydroge- nases in the citric acid cycle of Corynebacterium glutamicum. J Bacteriol. 2000, 182 (24), 6884-6891.
63. Kather, B.; Stingl, K.; van der Rest, M. E.; Altendorf, K.; Molenaar, D. Another unusual type of citric acid cycle enzyme in Helicobacter pylori: the malate:quinone oxidoreductase. J. Bacteriol. 2000, 182 (11), 3204-3209.
64. Ackerley, D. F.; Gonzalez, C. F.; Park, C. H.; Blake, R., 2nd; Keyhan, M.; Matin, A. Chromate-reducing properties of soluble flavoproteins from Pseudomonas putida and Escherichia coli. Appl. Environ. Microbiol. 2004, 70 (2), 873-882.
65. Gonzalez, C. F.; Ackerley, D. F.; Lynch, S. V.; Matin, A. ChrR, a soluble quinone reductase of Pseudomonas putida that defends against H2O2. J. Biol. Chem. 2005, 280 (24), 22590-22595.
66. Tam, R.; Saier, M. H. Structural, functional, and dvolutionary relationships among extracellular solute-binding recpetors of bacteria. Microbiol. Rev. 1993, 57 (2), 320-346.
67. Keskin, O.; Jernigan, R. L.; Bahar, I. Proteins with similar architecture exhibit similar large-scale dynamic behavior. Biophys. J. 2000, 78 (4), 2093-2106.
68. Sauer, U.; Eikmanns, B. J. The PEP-pyruvate-oxaloacetate node as the switch point for carbon flux distribution in bacteria. FEMS Microbiol. Rev. 2005, 29 (4), 765-794.
69. Pye, V. E.; Tingey, A. P.; Robson, R. L.; Moody, P. C. The structure and mechanism of serine acetyltransferase from Escherichia coli. J. Biol. Chem. 2004, 279 (39), 40729-40736.
70. Leyh, T. S.; Taylor, J. C.; Markham, G. D. The sulfate activation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization. J. Biol. Chem. 1988, 263 (5), 2409-2416.
71. Even, S.; Burguiere, P.; Auger, S.; Soutourina, O.; Danchin, A.; Martin-Verstraete, I. Global control of cysteine metabolism by CymR in Bacillus subtilis. J. Bacteriol. 2006, 188 (6), 2184-2197.
72. Lithgow, J. K.; Hayhurst, E. J.; Cohen, G.; Aharonowitz, Y.; Foster, S. J. Role of a cysteine synthase in Staphylococcus aureus. J. Bacteriol. 2004, 186 (6), 1579-1590.