Dosage-dependent proteome response of Shewanella oneidensis MR-1 to acute chromate challenge

Journal of Proteome Research

Volumn 6, Issue 5, 2007, Pages 1745-1757

  Thompson, Melissa R ^a,b   VerBerkmoes, Nathan C ^b   Chourey, Karuna ^c   Shah, Manesh ^b   Thompson, Dorothea K ^d   Hettich, Robert L ^b  

^a UNIVERSITY OF TENNESSEE   (United States)

^b OAK RIDGE NATIONAL LABORATORY   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

^d PURDUE UNIVERSITY   (United States)

Author keywords

Chromate stress; Linear trapping quadrupole; Mass spectrometry; Multidimensional liquid chromatography; Shewanella oneidensis; Shotgun proteomics

Indexed keywords

CHROMIC ACID; PROTEOME;

ARTICLE; DNA BINDING; ENERGY METABOLISM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIGH THROUGHPUT SCREENING; IRON TRANSPORT; MASS SPECTROMETRY; NUCLEOTIDE SEQUENCE; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEOMICS; SHEWANELLA ONEIDENSIS; STRESS; UNINDEXED SEQUENCE; UPREGULATION;

BACTERIAL PROTEINS; CHROMATES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPUTATIONAL BIOLOGY; DOSE-RESPONSE RELATIONSHIP, DRUG; MOLECULAR SEQUENCE DATA; PROTEOME; SHEWANELLA; TANDEM MASS SPECTROMETRY;

BACTERIA (MICROORGANISMS); SHEWANELLA ONEIDENSIS; SHEWANELLA ONEIDENSIS MR-1;

EID: 34249341301     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr060502x     Document Type: Article

References (47)

1. Washburn, M. P.; Wolters, D. A.; Yates, J. R., III. Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 2001, 19, 242-247.
2. McDonald, W. H.; Ohi, R.; Miyamoto, D. T.; Mitchison, T. J.; Yates, J. R., III. Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins fromcomplex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT. Int. J. Mass Spectrom. 2002, 219, 245-251.
3. Elias, D. A.; Monroe, M. E.; Smith, R. D.; Fredickson, J. K.; Lipton, M. S. Confirmation of the expression of a large set of conserved hypothetical proteins in Shewanella oneidensis MR-1. J. Microbiol. Methods 2006, 66(2), 223-33.
4. Jonscher, K. R.; Yates, J. R., III. The quadrupole ion trap mass spectrometer-a small solution to a big challenge. Anal. Biochem. 1997, 244, 1-15.
5. Kolker, E.; Purvine, S.; Galperin, M. Y.; Stolyar, S.; Goodlett, D. R.; Nesvizhskii, A. I.; Keller, A.; Xie, T.; Eng, J. K.; Yi, E.; Hood, L.; Picone, A. F.; Cherny, T.; Tjaden, B. C.; Siegel, A. F.; Reilly, T. J.; Makarova, K. S.; Paisson, B. O.; Smith, A. L. Initial proteome analysis of model microorganism Haemophilus influenzae strain Rd KW20. J. Bacteriol. 2003, 185, 4593-4602.
6. Florens, L.; Washburn, M. P.; Raine, J. D.; Anthony, R. M. Grainger, M.; Haynes, J. D.; Moch, J. K.; Muster, N.; Sacci, J. B. Tabb, D. L.; Witney, A. A.; Wolters, D. A.; Wu, Y.; Gardner, M. J. Holder, A. A.; Sinden, R. E.; Yates, J. R., III.; Carucci, D. J. A proteomic view of the Plasmodium falciparum life cycle. Nature 2002, 419, 520-526.
7. Romine, M. F.; Elias, D. A.; Monroe, M. E.; Auberry, K.; Fang, R.; Fredickson, J. K.; Anderson, G. A.; Smith, R. D.; Lipton, M. S. Validation of Shewanella oneidensis MR-1 small proteins by AMT tag-based proteome analysis. OMICS 2004, 8, 239-254.
8. Elias, D. A.; Monroe, M. E.; Marshall, M. J.; Romine, M. F.; Belieav, A. S.; Fredrickson, J. K.; Anderson, G. A.; Smith, R. D.; Lipton, M. S. Global detection and characterization of hypothetical proteins in Shewanella oneidensis MR-1 using LC-MS based proteomics. Proteomics 2005, 5, 3120-3130.
9. Schwartz, J. C.; Senko, M.; Syka, J. E. P. A two-dimensional quadrupole ion trap mass spectrometer. J. Am. Soc. Mass Spectrom. 2002, 13, 659-669.
10. Hu, Q.; Noll, R. J.; Li, H.; Makarov, A.; Hardman, M.; Cooks, R. G. The Orbitrap: a new mass spectrometer. J. Mass Spectrom. 2005, 40, 430-443.
11. 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, 1054-1071.
12. Chourey, K.; Thompson, M. R.; Morrell-Falvey, J.; Verberkmoes, N. C.; Brown, S. D.; Shah, M.; Hettich, R. L.; Zhou, J.; Doktycz, M.; Thompson, D. K. Global Molecular and Morphological Effects of 24-h Chromium Exposure on Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 2006, 72, 6331-6344.
13. Ram, R. J.; VerBerkmoes, N. C.; Thelen, M. P.; Tyson, G. W.; Baker, B. J.; Blake, R. C., II.; Shah, M.; Hettich, R. L.; Banfield, J. F. Community proteomics of a natural microbial biofilm. Science 2005, 308, 1915-1920.
14. Ding, Y. H.; Hixson, K. K.; Giometti, C. S.; Stanley, A.; Esteve-Nunez, A.; Khare, T.; Tollaksen, S. L.; Zhu, W.; Adkins, J. N.; Lipton, M. S.; Smith, R. D.; Mester, T.; Lovley, D. R. The proteome of dissimilatory metal-reducing microorganism Geobacter sulfurreducens under various growth conditions. Biochim. Biophys. Acta 2006, 1764 (7), 1198-1206.
15. James, B. R. The challenge of remediating chromium-contami-nated soil. Environ. Sci. Technol. 1996, 30, A248-A251.
16. Gadd, G. M. Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr. Opin. Biotechnol. 2000, 11, 271-9.
17. Myers, C. R.; Carstens, B. P.; Antholine, W. E.; Myers, J. M. Chromium(VI) reductase activity is associated with the cytoplasmic membrane of anaerobically grown Shewanella putrefaciens MR-1. J. Appl. Microbiol. 2000, 88, 98-106.
18. Viamajala, S.; Peyton, B. M.; Apel, W. A.; Petersen, J. N. Chromate/ nitrite interactions in Shewanella oneidensis MR-1: Evidence for multiple hexavalent chromium (CrfVI)] reduction mechanisms dependent on physiological growth conditions. Biotechnol. Bioeng. 2002, 78, 770-778.
19. Daulton, T. L.; Little, B. J.; Lowe, K.; Jones-Meehan, J. Electron energy loss spectroscopy techniques for the study of microbial Chromium(VI) reduction. J. Microbiol. Methods 2002, 50, 39-54.
20. Caccavo, F.; Ramsing, N. B.; Costerton, J. W. Morphological and metabolic responses to starvation by the dissimilatory metal-reducing bacterium Shewanella alga BrY. Appl. Environ. Microbiol. 1996, 62, 4678-4682.
21. Nyman, J. L.; Caccavo, F.; Cunningham, A. B.; Gerlach, R. Biogeochemical elimination of Chromium(VI) from contaminated water. Biorem. J. 2002, 6, 39-55.
22. Wielinga, B.; Mizuba, M. M.; Hansel, C. M.; Fendorf, S. Iron promoted reduction of chromate by dissimilatory iron-reducing bacteria. Environ. Sci. Technol. 2001, 35, 522-527.
23. Viamajala, S.; Peyton, B.; Sani, R.; Apel, W.; Petersen, J. Toxic effects of Chromium(VI) on anaerobic and aerobic growth of Shewanella ondeidensis MR-1. Biotechnol. Prog. 2004, 20, 87-95.
24. Middleton, S. S.; Latmani, R. B.; Mackey, M. R.; Ellisman, M. H.; Tebo, B. M.; Criddle, C. S. Cometabolism of Cr(VI) by Shewanella oneidensis MR-1 produces cell-associated reduced chromium and inhibits growth. Biotechnol. Bioeng. 2003, 83(6), 627-637.
25. Myers, C. R.; Nealson, K. H. Respiration-linked proton translocation coupled to anaerobic reduction of manganese(IV) and iron(III) in Shewanella putrefaciens MR-1. J. Bacteriol. 1990, 172(11), 6232-6238.
26. Bencheikh-Latmani, R.; Middleton Williams, S.; Haucke, L.; Criddle, C. S.; Wu, L.; Zhou, J.; Tebo, B. M. Global transcriptional profiling of Shewanella oneidensis MR-1 during Cr(VI) and U(VI) reduction. Appl. Environ. Microbiol. 2005, 71, 7453-7460.
27. Lovley, D. R.; Phillips, E. J. Reduction of Chromate by Desulfovibrio vulgaris and Its c(3) Cytochrome. Appl. Environ. Microbiol. 1994, 60(2), 726-728.
28. 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, 976-989.
29. Tabb, D. L.; McDonald, W. H.; Yates, J. R., III. DTASelect and Contrast: Tools for assembling and comparing protein identifications from shotgun proteomics. J. Proteome Res. 2002, 1, 21-26.
30. VerBerkmoes, N. C.; Shah, M. B.; Lankford, P. K.; Pelletier, D. A.; Strader, M. B.; Tabb, D. L.; McDonald, W. H.; Barton, J. W.; Hurst, G. B.; Hauser, L.; Davison, B. H.; Beatty, J. T.; Harwood, C. S.; Tabita, F. R.; Hettich, R. L.; Larimer, F. W. Determination and comparison of the baseline proteomes of the versatile microbe Rhodopseudomonas palustris under its major metabolic states. J. Proteome Res. 2006, 5, 287-298.
31. Peng, J.; Elias, J. E.; Thoreen, C. C.; Licklider, L. J.; Gygi, S. P. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2003, 2, 43-50.
32. Wan, X. F.; Verberkmoes, N. C.; McCue, L. A.; Stanek, D.; Connelly, H.; Hauser, L. J.; Wu, L.; Liu, X.; Yan, T.; Leaphart, A.; Hettich, R. L.; Zhou, J.; Thompson, D. K. Transcriptomic and proteomic characterization of the Fur modulon in the metal-reducing bacterium Shewanella oneidensis. J. Bacteriol. 2004, 186(24), 8385-8400.
33. Xie, H.; Griffin, T. J. Trade-off between high sensitivity and increased potential for false positive peptide sequence matches using a two-dimensional linear ion trap for tandem mass spectrometry-based proteomics. J. Proteome Res. 2006, 5, 1003-1009.
34. Riter, L. S.; Gooding, K. M.; Hodge, B. D.; Julian, R. K., Jr. Comparison of the Paul ion trap to the linear ion trap for use in global proteomics. Proteomics 2006, 6, 1735-1740.
35. Gygi, S. P.; Rist, B.; Gerber, S. A.; Turecek, F.; Gelb, M. H.; Aebersold, R. Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 1999, 17(10), 994-999.
36. Washburn, M. P.; Ulaszek, R.; Deciu, C.; Schieltz, D. M.; Yates, J. R., III. Analysis of quantitative proteomic data generated via multidimensional protein identification technology. Anal. Chem. 2002, 74, 1650-1657.
37. Luo, Q.; Shen, Y.; Hixson, K. K.; Zhao, R.; Yang, F.; Moore, R. J.; Mottaz, H. M.; Smith, R. D. Preparation of 20-μm-i.d. silica-based monolithic columns and their performance for proteomics analyses. Anal. Chem. 2005, 77, 5028-5035.
38. Alvarez, A. H.; Moreno-Sánchez, R.; Cervantes, C. Chromate efflux by means of the ChrA chromate resistance protein from Pseudomonas aeruginosa. J. Bacteriol. 1999, 181, 7398-7400.
39. Cervantes, C.; Campos-Garcia, J.; Devars, S.; Gutierrez-Corona, F.; Loza-Tavera, H.; Torres-Guzman, J. C.; Moreno-Sanchez, R. Interactions of chromium with microorganisms and plants. FEMS Microbiol. Rev. 2001, 25, 335-347.
40. Muskotal, A.; Kiraly, R.; Sebestyen, A.; Gugolya, Z.; Vegh, B. M.; Vonderviszt, F. Interaction of FliS flagellar chaperone with flagellin. FEBS Lett. 2006, 580(16), 3916-3920.
41. Ohtake, H.; Cervantes, C.; Silver, S. Decreased chromate uptake in Pseudomonas fluorescens carrying a chromate resistance plasmid. J. Bacteriol. 1987, 169, 3853-3556.
42. Nies, A.; Nies, D. H.; Silver, S. Cloning and expression of plasmid genes encoding resistances to chromate and cobalt in Alcaligenes eutrophus. J. Bacteriol. 1989, 171, 5065-5070.
43. Suzuki, T.; Miyata, N.; Horitsu, H.; Kawai, K.; Takamizawa, K.; Tai, Y.; Okazaki, M. NAD(P)H-dependent chromium (VI) reductase of Pseudomonas ambigua G-1: a Cr(V) intermediate is formed during the reduction of Cr(VI) to Cr(III). J. Bacteriol. 1992, 174(16), 5340-5345.
44. Thomas, J. G.; Baneyx, F. Roles of the Escherichia coli small heat shock proteins IbpA and IbpB in thermal stress management: comparison with ClpA, ClpB, and HtpG in vivo. J. Bacteriol. 1998, 180, 5165-5172.
45. Jiang, X.; Zhang, M.; Ding, Y.; Yao, J.; Chen, H.; Zhu, D.; Muramatu, M. Escherichia coli prlC gene encodes a trypsin-like proteinase regulating the cell cycle. J. Biochem. (Tokyo) 1998, 124(5), 980-985.
46. Weber, A.; Kogl, S. A.; Jung, K. Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J. Bacteriol. 2006,188 (20), 7165-7175.
47. Bladder, A. R.; Hammer, A. A.; MacCoss, M. J.; Wu, C. C. Quantitative comparison of proteomic data quality between a 2D and 3D quadrupole ion trap. Anal. Chem. 2006, 78(4), 1337-1344.