Sulfur-34S stable isotope labeling of amino acids for quantification (SULAQ34) of proteomic changes in pseudomonas fluorescens during naphthalene degradation

Molecular and Cellular Proteomics

Volumn 12, Issue 8, 2013, Pages 2060-2069

  Herbst, Florian Alexander ^a,b   Taubert, Martin ^a,c   Jehmlich, Nico ^a,d   Behr, Tobias ^e   Schmidt, Frank ^a   Von Bergen, Martin ^a,f   Seifert, Jana ^a,g  

^a HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^d UNIVERSITY OF GREIFSWALD   (Germany)

^e Hochschule Wismar   (Germany)

^f AALBORG UNIVERSITY   (Denmark)

^g UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CARBON 13; NAPHTHALENE; RADIOISOTOPE; SULFUR 34S; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; NAPHTHALENE DERIVATIVE; POLLUTANT; SULFUR;

ARTICLE; BACTERIAL METABOLISM; CELL CULTURE; DEGRADATION; ISOTOPE LABELING; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; PSEUDOMONAS FLUORESCENS; QUANTITATIVE ANALYSIS; BIOREMEDIATION; CHEMISTRY; METABOLISM; POLLUTANT;

AMINO ACIDS; BACTERIAL PROTEINS; BIODEGRADATION, ENVIRONMENTAL; ENVIRONMENTAL POLLUTANTS; ISOTOPE LABELING; NAPHTHALENES; PROTEOMICS; PSEUDOMONAS FLUORESCENS; SULFUR ISOTOPES;

EID: 84881102933     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.025627     Document Type: Article

References (57)

1. Schulze, W. X., and Usadel, B. (2010) Quantitation in mass-spectrometrybased proteomics. Annu. Rev. Plant Biol. 61, 491-516
2. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
3. Schmidt, F., Scharf, S. S., Hildebrandt, P., Burian, M., Bernhardt, J., Dhople, V., Kalinka, J., Gutjahr, M., Hammer, E., and Völker, U. (2010) Time-resolved quantitative proteome profiling of host-pathogen interactions: the response of Staphylococcus aureus RN1HG to internalisation by human airway epithelial cells. Proteomics 10, 2801-2811
4. Soufi, B., Kumar, C., Gnad, F., Mann, M., Mijakovic, I., and Macek, B. (2010) Stable isotope labeling by amino acids in cell culture (SILAC) applied to quantitative proteomics of Bacillus subtilis. J. Proteome Res. 9, 3638-3646
5. Otto, A., Bernhardt, J., Meyer, H., Schaffer, M., Herbst, F. A., Siebourg, J., Mader, U., Lalk, M., Hecker, M., and Becher, D. (2010) Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis. Nat. Commun. 1, 137
6. Jehmlich, N., Kopinke, F. D., Lenhard, S., Vogt, C., Herbst, F. A., Seifert, J., Lissner, U., Völker, U., Schmidt, F., and von Bergen, M. (2012) Sulfur-36S stable isotope labeling of amino acids for quantification (SULAQ). Proteomics 12, 37-42
7. Wang, M., Feng, W., Lu, W., Li, B., Wang, B., Zhu, M., Wang, Y., Yuan, H., Zhao, Y., and Chai, Z. (2007) Quantitative analysis of proteins via sulfur determination by HPLC coupled to isotope dilution ICPMS with a hexapole collision cell. Anal. Chem. 79, 9128-9134
8. Pfeffer, M., Maurer, M., Kollensperger, G., Hann, S., Graf, A. B., and Mattanovich, D. (2011) Modeling and measuring intracellular fluxes of secreted recombinant protein in Pichia pastoris with a novel 34S labeling procedure. Microb. Cell Fact. 10, 47
9. Nikolaev, E. N., Jertz, R., Grigor'ev, A. S., and Baykut, G. (2012) Fine structure in isotopic peak distributions measured using dynamically harmonized FT ICR cell at 7 Tesla. Anal. Chem. 84, 2275-2283
10. Lalucat, J., Bennasar, A., Bosch, R., Garcia-Valdes, E., and Palleroni, N. J. (2006) Biology of Pseudomonas stutzeri. Microbiol. Mol. Biol. Rev. 70, 510-547
11. Jeyalakshmi, D., and Kanmani, S. (2008) Bioremediation of chromium contaminated soil by Pseudomonas fluorescens and indigenous microorganisms. J. Environ. Sci. Eng. 50, 1-6
12. Guazzaroni, M.-E., Herbst, F.-A., Lores, I., Tamames, J., Peláez, A. I., López-Cortés, N., Alcaide, M., Del Pozo, M. V., Vieites, J. M., von Bergen, M., Gallego, J. L. R., Bargiela, R., López-López, A., Pieper, D. H., Rosselló-Móra, R., Sánchez, J., Seifert, J., and Ferrer, M. (2013) Metaproteogenomic insights beyond bacterial response to naphthalene exposure and bio-stimulation. ISME J. 7, 122-136
13. Peng, R. H., Xiong, A. S., Xue, Y., Fu, X. Y., Gao, F., Zhao, W., Tian, Y. S., and Yao, Q. H. (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol. Rev. 32, 927-955
14. Widdel, F., Kohring, G. W., and Mayer, F. (1983) Studies on dissimilatory sulfate-reducing bacteria that decompose fatty-Acids . Characterization of the filamentous gliding Desulfonema-Limicola Gen-Nov Sp-Nov, and Desulfonema-Magnum Sp-Nov. Arch. Microbiol. 134, 286-294
15. Widdel, F., and Pfennig, N. (1981) Studies on dissimilatory sulfate-reducing bacteria that decompose fatty-Acids . Isolation of new sulfate-reducing bacteria enriched with acetate from saline environments- description of Desulfobacter-Postgatei Gen-Nov, Sp-Nov. Arch. Microbiol. 129, 395-400
16. Jehmlich, N., Schmidt, F., Hartwich, M., von Bergen, M., Richnow, H. H., and Vogt, C. (2008) Incorporation of carbon and nitrogen atoms into proteins measured by protein-based stable isotope probing (Protein- SIP). Rapid Commun. Mass Spectrom. 22, 2889-2897
17. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
18. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A., Olsen, J. V., and Mann, M. (2011) Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10, 1794-1805
19. Kessner, D., Chambers, M., Burke, R., Agus, D., and Mallick, P. (2008) ProteoWizard: open source software for rapid proteomics tools development. Bioinformatics 24, 2534-2536
20. Hoopmann, M. R., MacCoss, M. J., and Moritz, R. L. (2012) Identification of peptide features in precursor spectra using Hardklor and Kronik. Curr. Protoc. Bioinformatics Chapter 13, Unit 18
21. Rabus, R., Jack, D. L., Kelly, D. J., and Saier, M. H., Jr. (1999) TRAP transporters: an ancient family of extracytoplasmic solute-receptor-dependent secondary active transporters. Microbiology 145(Pt 12), 3431-3445
22. Weber, H., Polen, T., Heuveling, J., Wendisch, V. F., and Hengge, R. (2005) Genome-wide analysis of the general stress response network in Escherichia coli: sigmaS-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol. 187, 1591-1603
23. Segura, A., Godoy, P., van Dillewijn, P., Hurtado, A., Arroyo, N., Santacruz, S., and Ramos, J. L. (2005) Proteomic analysis reveals the participation of energy- and stress-related proteins in the response of Pseudomonas putida DOT-T1E to toluene. J. Bacteriol. 187, 5937-5945
24. Barnsley, E. A. (1976) Role and regulation of the ortho and meta pathways of catechol metabolism in pseudomonads metabolizing naphthalene and salicylate. J. Bacteriol. 125, 404-408
25. Shamsuzzaman, K. M., and Barnsley, E. A. (1974) The regulation of naphthalene metabolism in pseudomonads. Biochem. Biophys. Res. Commun. 60, 582-589
26. Persson, B., Hedlund, J., and Jornvall, H. (2008) Medium- and short-chain dehydrogenase/reductase gene and protein families: the MDR superfamily. Cell. Mol. Life Sci. 65, 3879-3894
27. Nishimura, M., Kohno, K., Nishimura, Y., Inagaki, M., and Davies, J. (2011) Characterization of two isozymes of coniferyl alcohol dehydrogenase from Streptomyces sp. NL15-2K. Biosci. Biotechnol. Biochem. 75, 1770-1777
28. Guyard-Nicodeme, M., Bazire, A., Hemery, G., Meylheuc, T., Molle, D., Orange, N., Fito-Boncompte, L., Feuilloley, M., Haras, D., Dufour, A., and Chevalier, S. (2008) Outer membrane modifications of Pseudomonas fluorescens MF37 in response to hyperosmolarity. J. Proteome Res. 7, 1218-1225
29. Segura, A., Molina, L., Fillet, S., Krell, T., Bernal, P., Munoz-Rojas, J., and Ramos, J. L. (2011) Solvent tolerance in Gram-negative bacteria. Curr. Opin. Biotechnol. 23, 415-421
30. Wick, L. Y., Pasche, N., Bernasconi, S. M., Pelz, O., and Harms, H. (2003) Characterization of multiple-substrate utilization by anthracene-degrading Mycobacterium frederiksbergense LB501T. Appl. Environ. Microbiol. 69, 6133-6142
31. Hearn, E. M., Dennis, J. J., Gray, M. R., and Foght, J. M. (2003) Identification and characterization of the emhABC efflux system for polycyclic aromatic hydrocarbons in Pseudomonas fluorescens cLP6a. J. Bacteriol. 185, 6233-6240
32. Obi, I. R., Nordfelth, R., and Francis, M. S. (2011) Varying dependency of periplasmic peptidylprolyl cis-trans isomerases in promoting Yersinia pseudotuberculosis stress tolerance and pathogenicity. Biochem. J. 439, 321-332
33. Justice, S. S., Hunstad, D. A., Harper, J. R., Duguay, A. R., Pinkner, J. S., Bann, J., Frieden, C., Silhavy, T. J., and Hultgren, S. J. (2005) Periplasmic peptidyl prolyl cis-trans isomerases are not essential for viability, but SurA is required for pilus biogenesis in Escherichia coli. J. Bacteriol. 187, 7680-7686
34. Henderson, B., and Martin, A. (2011) Bacterial moonlighting proteins and bacterial virulence. Curr. Top. Microbiol. Immunol. 358, 155-213
35. Doyle, S. M., and Wickner, S. (2009) Hsp104 and ClpB: protein disaggregating machines. Trends Biochem. Sci. 34, 40-48
36. Acebron, S. P., Martin, I., del Castillo, U., Moro, F., and Muga, A. (2009) DnaK-mediated association of ClpB to protein aggregates. A bichaperone network at the aggregate surface. FEBS Lett. 583, 2991-2996
37. Lara-Ortiz, T., Castro-Dorantes, J., Ramirez-Santos, J., and Gomez-Eichelmann, M. C. (2012) Role of the DnaK-ClpB bichaperone system in DNA gyrase reactivation during a severe heat-shock response in Escherichia coli. Can. J. Microbiol. 58, 195-199
38. Park, S. K., Jin, E. S., and Lee, M. Y. (2008) Expression and antioxidant enzymes in Chaetoceros neogracile, an Antarctic alga. Cryo Letters 29, 351-361
39. Steeves, C. H., Potrykus, J., Barnett, D. A., and Bearne, S. L. (2011) Oxidative stress response in the opportunistic oral pathogen Fusobacterium nucleatum. Proteomics 11, 2027-2037
40. Okano, S., Shibata, Y., Shiroza, T., and Abiko, Y. (2006) Proteomics-based analysis of a counter-oxidative stress system in Porphyromonas gingivalis. Proteomics 6, 251-258
41. Thomas, J. G., and Baneyx, F. (2000) ClpB and HtpG facilitate de novo protein folding in stressed Escherichia coli cells. Mol. Microbiol. 36, 1360-1370
42. Lindner, A. B., Madden, R., Demarez, A., Stewart, E. J., and Taddei, F. (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc. Natl. Acad. Sci. U.S.A. 105, 3076-3081
43. de Groot, N. S., and Ventura, S. (2010) Protein aggregation profile of the bacterial cytosol. PLoS One 5, e9383
44. Missiakas, D., Schwager, F., Betton, J. M., Georgopoulos, C., and Raina, S. (1996) Identification and characterization of HsIV HsIU (ClpQ ClpY) proteins involved in overall proteolysis of misfolded proteins in Escherichia coli. EMBO J. 15, 6899-6909
45. Cheng, C. H., and Lee, W. C. (2010) Protein solubility and differential proteomic profiling of recombinant Escherichia coli overexpressing double- tagged fusion proteins. Microb. Cell Fact. 9, 63
46. Zou, C. G., Xu, Y. F., Liu, W. J., Zhou, W., Tao, N., Tu, H. H., Huang, X. W., Yang, J. K., and Zhang, K. Q. (2010) Expression of a serine protease gene prC is up-regulated by oxidative stress in the fungus Clonostachys rosea: implications for fungal survival. PLoS One 5, e13386
47. Gur, E., and Sauer, R. T. (2008) Recognition of misfolded proteins by Lon, a AAA(-) protease. Genes Dev. 22, 2267-2277
48. Sakoh, M., Ito, K., and Akiyama, Y. (2005) Proteolytic activity of HtpX, a membrane-bound and stress-controlled protease from Escherichia coli. J. Biol. Chem. 280, 33305-33310
49. Koharyova, M., and Kolarova, M. (2008) Oxidative stress and thioredoxin system. Gen. Physiol. Biophys. 27, 71-84
50. Masip, L., Veeravalli, K., and Georgiou, G. (2006) The many faces of glutathione in bacteria. Antioxid. Redox Signal. 8, 753-762
51. May, D. W. (1901) Catalase, a new enzym of general occurrence. Science 14, 815-816
52. Engelmann, S., and Hecker, M. (1996) Impaired oxidative stress resistance of Bacillus subtilis sigB mutants and the role of katA and katE. FEMS Microbiol. Lett. 145, 63-69
53. Donati, A. J., Jeon, J. M., Sangurdekar, D., So, J. S., and Chang, W. S. (2011) Genome-wide transcriptional and physiological responses of Bradyrhizobium japonicum to paraquat-mediated oxidative stress. Appl. Environ. Microbiol. 77, 3633-3643
54. Wolf, C., Hochgrafe, F., Kusch, H., Albrecht, D., Hecker, M., and Engelmann, S. (2008) Proteomic analysis of antioxidant strategies of Staphylococcus aureus: diverse responses to different oxidants. Proteomics 8, 3139-3153
55. Emri, T., Pocsi, I., and Szentirmai, A. (1999) Analysis of the oxidative stress response of Penicillium chrysogenum to menadione. Free Radic. Res. 30, 125-132
56. Mailloux, R. J., Lemire, J., and Appanna, V. D. (2011) Metabolic networks to combat oxidative stress in Pseudomonas fluorescens. Antonie Van Leeuwenhoek 99, 433-442
57. Vasiliou, V., Pappa, A., and Petersen, D. R. (2000) Role of aldehyde dehydrogenases in endogenous and xenobiotic metabolism. Chem. Biol. Interact. 129, 1-19