Comparative proteomic and metabolomic analysis of Staphylococcus warneri SG1 cultured in the presence and absence of butanol

Journal of Proteome Research

Volumn 12, Issue 10, 2013, Pages 4478-4489

  Fu, Feifei ^a   Cheng, Victor W T ^a   Wu, Yiman ^a   Tang, Yanan ^a   Weiner, Joel H ^a   Li, Liang ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

bacterium; butanol; quantitative metabolomics; quantitative proteomics; solvent tolerance; Staphylococcus warneri SG1

Indexed keywords

BUTANOL; CHAPERONE;

ARTICLE; BACTERIAL MEMBRANE; BACTERIUM CULTURE; BIOGENESIS; COMPARATIVE STUDY; ENERGY METABOLISM; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABOLOMICS; METHYLATION; NONHUMAN; OPEN READING FRAME; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEOMICS; STAPHYLOCOCCUS WARNERI;

ADAPTATION, PHYSIOLOGICAL; AMINES; BACTERIAL PROTEINS; BUTANOLS; CARBOXYLIC ACIDS; CELL MEMBRANE; CITRIC ACID CYCLE; ENERGY METABOLISM; METABOLOME; METABOLOMICS; MICROBIAL VIABILITY; PHENOLS; PROTEOME; PROTEOMICS; STAPHYLOCOCCUS; STRESS, PHYSIOLOGICAL;

EID: 84885216277     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400533m     Document Type: Article

References (77)

1. Sikkema, J.; de Bont, J. A.; Poolman, B. Mechanisms of membrane toxicity of hydrocarbons Microbiol. Rev. 1995, 59 (2) 201-22
2. Isken, S.; de Bont, J. A. M. Bacteria tolerant to organic solvents Extremophiles 1998, 2 (3) 229-238
3. Sardessai, Y.; Bhosle, S. Tolerance of bacteria to organic solvents Res. Microbiol. 2002, 153 (5) 263-268
4. Ramos, J. L.; Duque, E.; Gallegos, M. T.; Godoy, P.; Ramos-Gonzalez, M. I.; Rojas, A.; Teran, W.; Segura, A. Mechanisms of solvent tolerance in Gram-negative bacteria Ann. Rev. Microbiol. 2002, 56, 743-768
5. Nicolaou, S. A.; Gaida, S. M.; Papoutsakis, E. T. A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation Metab. Eng. 2010, 12 (4) 307-331
6. Segura, A.; Molina, L.; Fillet, S.; Krell, T.; Bernal, P.; Munoz-Rojas, J.; Ramos, J. L. Solvent tolerance in Gram-negative bacteria Curr. Opin. Biotechnol. 2012, 23 (3) 415-421
7. Nielsen, L. E.; Kadavy, D. R.; Rajagopal, S.; Drijber, R.; Nickerson, K. W. Survey of extreme solvent tolerance in Gram-positive cocci: membrane fatty acid changes in Staphylococcus haemolyticus grown in toluene Appl. Environ. Microbiol. 2005, 71 (9) 5171-5176
8. Zahir, Z.; Seed, K. D.; Dennis, J. J. Isolation and characterization of novel organic solvent-tolerant bacteria Extremophiles 2006, 10 (2) 129-138
9. Grandvalet, C.; Assad-Garcia, J. S.; Chu-Ky, S.; Tollot, M.; Guzzo, J.; Gresti, J.; Tourdot-Marechal, R. Changes in membrane lipid composition in ethanol- and acid-adapted Oenococcus oeni cells: characterization of the cfa gene by heterologous complementation Microbiology 2008, 154 (Pt 9) 2611-2619
10. Gao, Y.; Dai, J.; Peng, H.; Liu, Y.; Xu, T. Isolation and characterization of a novel organic solvent-tolerant Anoxybacillus sp. PGDY12, a thermophilic Gram-positive bacterium J. Appl. Microbiol. 2011, 110 (2) 472-478
11. Cheng, V. W.; Zhang, G.; Oyedotun, K. S.; Ridgway, D.; Ellison, M. J.; Weiner, J. H. Complete Genome of the Solvent-Tolerant Staphylococcus warneri Strain SG1 Genome Announce. 2013, 1 (2) e0003813
12. Jones, D.; Woods, D. Acetone-butanol fermentation revisited Microbiol. Rev. 1986, 50, 484-524
13. Bermejo, L. L.; Welker, N. E.; Papoutsakis, E. T. Expression of Clostridium acetobutylicum ATCC 824 genes in Escherichia coli for acetone production and acetate detoxification Appl. Environ. Microbiol. 1998, 64 (3) 1079-1085
14. Steen, E.; Chan, R.; Prasad, N.; Myers, S.; Petzold, C.; Redding, A.; Ouellet, M.; Keasling, J. Metabolic engineering of Saccharomyces cerevisiae for the production of n-butanol Microb. Cell Fact. 2008, 7-36
15. Atsumi, S.; Cann, A.; Connor, M.; Shen, C.; Smith, K.; Brynildsen, M.; Chou, K.; Hanai, T.; Liao, J. Metabolic engineering of Escherichia coli for 1-butanol production Metab. Eng. 2008, 10, 305-311
16. Atsumi, S.; Hanai, T.; Liao, J. C. Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels Nature 2008, 451 (7174) 86-89
17. Tomas, C. A.; Beamish, J.; Papoutsakis, E. T. Transcriptional analysis of butanol stress and tolerance in Clostridium acetobutylicum J. Bacteriol. 2004, 186 (7) 2006-2018
18. Brynildsen, M. P.; Liao, J. C. An integrated network approach identifies the isobutanol response network of Escherichia coli Mol. Syst. Biol. 2009, 5, 277
19. Alsaker, K. V.; Paredes, C.; Papoutsakis, E. T. Metabolite stress and tolerance in the production of biofuels and chemicals: gene-expression-based systems analysis of butanol, butyrate, and acetate stresses in the anaerobe Clostridium acetobutylicum Biotechnol. Bioeng. 2010, 105 (6) 1131-1147
20. Mao, S.; Luo, Y.; Zhang, T.; Li, J.; Bao, G.; Zhu, Y.; Chen, Z.; Zhang, Y.; Li, Y.; Ma, Y. Proteome Reference Map and Comparative Proteomic Analysis between a Wild Type Clostridium acetobutylicum DSM 1731 and its Mutant with Enhanced Butanol Tolerance and Butanol Yield J. Proteome Res. 2010, 9 (6) 3046-3061
21. Mao, S.; Luo, Y.; Bao, G.; Zhang, Y.; Li, Y.; Ma, Y. Comparative analysis on the membrane proteome of Clostridium acetobutylicum wild type strain and its butanol-tolerant mutant Mol. BioSyst. 2011, 7 (5) 1660-1677
22. Segura, A.; Godoy, P.; van Dillewijn, P.; Hurtado, A.; Arroyo, N.; Santacruz, S.; Ramos, J. L. Proteomic analysis reveals the participation of energy- and stress-related proteins in the response of Pseudomonas putida DOT-T1E to toluene J. Bacteriol. 2005, 187 (17) 5937-5945
23. Wijte, D.; van Baar, B. L.; Heck, A. J.; Altelaar, A. F. Probing the proteome response to toluene exposure in the solvent tolerant Pseudomonas putida S12 J. Proteome Res. 2011, 10 (2) 394-403
24. Guo, K.; Li, L. Differential 12C-/13C-Isotope Dansylation Labeling and Fast Liquid Chromatography/Mass Spectrometry for Absolute and Relative Quantification of the Metabolome Anal. Chem. 2009, 81 (10) 3919-3932
25. Guo, K.; Li, L. High-Performance Isotope Labeling for Profiling Carboxylic Acid-Containing Metabolites in Biofluids by Mass Spectrometry Anal. Chem. 2010, 82 (21) 8789-8793
26. Ye, X.; Li, L. Microwave-Assisted Protein Solubilization for Mass Spectrometry-Based Shotgun Proteome Analysis Anal. Chem. 2012, 84 (14) 6181-6191
27. Wang, N.; Xie, C.; Young, J. B.; Li, L. Off-Line Two-Dimensional Liquid Chromatography with Maximized Sample Loading to Reversed-Phase Liquid Chromatography-Electrospray Ionization Tandem Mass Spectrometry for Shotgun Proteome Analysis Anal. Chem. 2009, 81 (3) 1049-1060
28. Wang, N.; Li, L. Exploring the Precursor Ion Exclusion Feature of Liquid Chromatography-Electrospray Ionization Quadrupole Time-of-Flight Mass Spectrometry for Improving Protein Identification in Shotgun Proteome Analysis Anal. Chem. 2008, 80 (12) 4696-4710
29. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4 (3) 207-214
30. Ishihama, Y.; Oda, Y.; Tabata, T.; Sato, T.; Nagasu, T.; Rappsilber, J.; Mann, M. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein Mol. Cell. Proteomics 2005, 4 (9) 1265-1272
31. Ji, C.; Guo, N.; Li, L. Differential dimethyl labeling of N-termini of peptides after guanidination for proteome analysis J. Proteome Res. 2005, 4 (9) 2099-2108
32. Lo, A.; Tang, Y.; Chen, L.; Li, L. Automation of dimethylation after guanidination labeling chemistry and its compatibility with common buffers and surfactants for mass spectrometry-based shotgun quantitative proteome analysis Anal. Chim. Acta 2013, 788 (0) 81-88
33. Wang, P.; Lo, A.; Young, J. B.; Song, J. H.; Lai, R.; Kneteman, N. M.; Hao, C. H.; Li, L. Targeted Quantitative Mass Spectrometric Identification of Differentially Expressed Proteins between Bax-Expressing and Deficient Colorectal Carcinoma Cells J. Proteome Res. 2009, 8 (7) 3403-3414
34. Tian, X.; Chen, L.; Wang, J.; Qiao, J.; Zhang, W. Quantitative proteomics reveals dynamic responses of Synechocystis sp. PCC 6803 to next-generation biofuel butanol J. Proteomics 2013, 78, 326-345
35. Hilger, M.; Mann, M. Triple SILAC to determine stimulus specific interactions in the Wnt pathway J. Proteome Res. 2012, 11 (2) 982-994
36. Tatusov, R. L.; Galperin, M. Y.; Natale, D. A.; Koonin, E. V. The COG database: a tool for genome-scale analysis of protein functions and evolution Nucleic Acids Res. 2000, 28 (1) 33-36
37. Ogata, H.; Goto, S.; Sato, K.; Fujibuchi, W.; Bono, H.; Kanehisa, M. KEGG: Kyoto Encyclopedia of Genes and Genomes Nucleic Acids Res. 1999, 27 (1) 29-34
38. Wu, Y. M.; Li, L. Determination of Total Concentration of Chemically Labeled Metabolites as a Means of Metabolome Sample Normalization and Sample Loading Optimization in Mass Spectrometry-Based Metabolomics Anal. Chem. 2012, 84 (24) 10723-10731
39. Smith, C. A.; Want, E. J.; O'Maille, G.; Abagyan, R.; Siuzdak, G. XCMS: Processing Mass Spectrometry Data for Metabolite Profiling Using Nonlinear Peak Alignment, Matching, and Identification Anal. Chem. 2006, 78 (3) 779-787
40. Guo, K.; Peng, J.; Zhou, R.; Li, L. Ion-pairing reversed-phase liquid chromatography fractionation in combination with isotope labeling reversed-phase liquid chromatography-mass spectrometry for comprehensive metabolome profiling J. Chromatogr., A 2011, 1218 (23) 3689-3694
41. Sivagnanam, K.; Raghavan, V.; Shah, M.; Hettich, R.; Verberkmoes, N.; Lefsrud, M. Comparative shotgun proteomic analysis of Clostridium acetobutylicum from butanol fermentation using glucose and xylose Proteome Sci. 2011, 9 (1) 66
42. Becher, D.; Hempel, K.; Sievers, S.; Zuhlke, D.; Pane-Farre, J.; Otto, A.; Fuchs, S.; Albrecht, D.; Bernhardt, J.; Engelmann, S.; Volker, U.; van Dijl, J. M.; Hecker, M. A proteomic view of an important human pathogen - towards the quantification of the entire Staphylococcus aureus proteome PLoS One 2009, 4 (12) e8176
43. Hempel, K.; Herbst, F.-A.; Moche, M.; Hecker, M.; Becher, D. Quantitative proteomic view on secreted, cell surface-associated, and cytoplasmic proteins of the methicillin-resistant human pathogen Staphylococcus aureus under iron-limited conditions J. Proteome Res. 2011, 10 (4) 1657-1666
44. Tatusov, R. L.; Galperin, M. Y.; Natale, D. A.; Koonin, E. V. The COG database: a tool for genome-scale analysis of protein functions and evolution Nucleic Acids Res. 2000, 28 (1) 33-36
45. Rutherford, B. J.; Dahl, R. H.; Price, R. E.; Szmidt, H. L.; Benke, P. I.; Mukhopadhyay, A.; Keasling, J. D. Functional genomic study of exogenous n-butanol stress in Escherichia coli Appl. Environ. Microbiol. 2010, 76 (6) 1935-1945
46. Schindler, C. A.; Schuhardt, V. T. Lysostaphin: A New Bacteriolytic Agent for the Staphylococcus Proc. Natl. Acad. Sci. U.S.A. 1964, 51, 414-21
47. Browder, H. P.; Zygmunt, W. A.; Young, J. R.; Tavormina, P. A. Lysostaphin: Enzymatic Mode of Action Biochem. Biophys. Res. Commun. 1965, 19, 383-389
48. Silhavy, T. J.; Kahne, D.; Walker, S. The bacterial cell envelope Cold Spring Harbor Perspect. Biol. 2010, 2 (5) a000414
49. Reith, J.; Mayer, C. Peptidoglycan turnover and recycling in Gram-positive bacteria Appl. Microbiol. Biotechnol. 2011, 92 (1) 1-11
50. Weidenmaier, C.; Peschel, A. Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions Nat. Rev. Microbiol. 2008, 6 (4) 276-287
51. Pepi, M.; Heipieper, H. J.; Fischer, J.; Ruta, M.; Volterrani, M.; Focardi, S. E. Membrane fatty acids adaptive profile in the simultaneous presence of arsenic and toluene in Bacillus sp. ORAs2 and Pseudomonas sp. ORAs5 strains Extremophiles 2008, 12 (3) 343-349
52. Lu, Y. J.; Zhang, Y. M.; Grimes, K. D.; Qi, J.; Lee, R. E.; Rock, C. O. Acyl-phosphates initiate membrane phospholipid synthesis in Gram-positive pathogens Mol. Cell 2006, 23 (5) 765-772
53. Yoshimura, M.; Oshima, T.; Ogasawara, N. Involvement of the YneS/YgiH and PlsX proteins in phospholipid biosynthesis in both Bacillus subtilis and Escherichia coli BMC Microbiol. 2007, 7 (1) 69
54. Cartwright, C. P.; Juroszek, J.-R.; Beavan, M. J.; Ruby, F. M. S.; De Morais, S. M. F.; Rose, A. H. Ethanol Dissipates the Proton-motive Force across the Plasma Membrane of Saccharomyces cerevisiae J. Gen. Microbiol. 1986, 132 (2) 369-377
55. Leao, C.; Van Uden, N. Effects of ethanol and other alkanols on passive proton influx in the yeast Saccharomyces cerevisiae Biochim. Biophys. Acta 1984, 774 (1) 43-48
56. Bowles, L. K.; Ellefson, W. L. Effects of butanol on Clostridium acetobutylicum Appl. Environ. Microbiol. 1985, 50 (5) 1165-1170
57. Volkers, R. J.; de Jong, A. L.; Hulst, A. G.; van Baar, B. L.; de Bont, J. A.; Wery, J. Chemostat-based proteomic analysis of toluene-affected Pseudomonas putida S12 Environ. Microbiol. 2006, 8 (9) 1674-1679
58. Torres, S.; Pandey, A.; Castro, G. R. Organic solvent adaptation of Gram positive bacteria: applications and biotechnological potentials Biotechnol. Adv. 2011, 29 (4) 442-452
59. Nicolaou, S. a.; Gaida, S. M.; Papoutsakis, E. T. A comparative view of metabolite and substrate stress and tolerance in microbial bioprocessing: From biofuels and chemicals, to biocatalysis and bioremediation Metab. Eng. 2010, 12 (4) 307-331
60. Yuvaniyama, P.; Agar, J. N.; Cash, V. L.; Johnson, M. K.; Dean, D. R. NifS-directed assembly of a transient [2Fe-2S] cluster within the NifU protein Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (2) 599-604
61. Smith, A. D.; Jameson, G. N.; Dos Santos, P. C.; Agar, J. N.; Naik, S.; Krebs, C.; Frazzon, J.; Dean, D. R.; Huynh, B. H.; Johnson, M. K. NifS-mediated assembly of [4Fe-4S] clusters in the N- and C-terminal domains of the NifU scaffold protein Biochemistry 2005, 44 (39) 12955-12969
62. Frees, D.; Qazi, S. N.; Hill, P. J.; Ingmer, H. Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence Mol. Microbiol. 2003, 48 (6) 1565-1578
63. Michel, A.; Agerer, F.; Hauck, C. R.; Herrmann, M.; Ullrich, J.; Hacker, J.; Ohlsen, K. Global regulatory impact of ClpP protease of Staphylococcus aureus on regulons involved in virulence, oxidative stress response, autolysis, and DNA repair J. Bacteriol. 2006, 188 (16) 5783-5796
64. Tomas, C. A.; Beamish, J.; Papoutsakis, E. T. Transcriptional analysis of butanol stress and tolerance in Clostridium acetobutylicum J. Bacteriol. 2004, 186 (7) 2006-2018
65. Boschi-Muller, S.; Olry, A.; Antoine, M.; Branlant, G. The enzymology and biochemistry of methionine sulfoxide reductases Biochim. Biophys. Acta 2005, 1703 (2) 231-238
66. Sasindran, S. J.; Saikolappan, S.; Dhandayuthapani, S. Methionine sulfoxide reductases and virulence of bacterial pathogens Future Microbiol. 2007, 2 (6) 619-630
67. Kumsta, C.; Jakob, U. Redox-regulated chaperones Biochemistry 2009, 48 (22) 4666-4676
68. Poole, L. B. Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases Arch. Biochem. Biophys. 2005, 433 (1) 240-254
69. Kang, I. H.; Kim, J. S.; Kim, E. J.; Lee, J. K. Cadaverine protects Vibrio vulnificus from superoxide stress J. Microbiol. Biotechnol. 2007, 17 (1) 176-179
70. Ha, H. C.; Sirisoma, N. S.; Kuppusamy, P.; Zweier, J. L.; Woster, P. M.; Casero, R. A. The natural polyamine spermine functions directly as a free radical scavenger Proc. Natl. Acad. Sci. U.S.A. 1998, 95 (19) 11140-11145
71. Brown, A. D. Inhibition by spermine of the action of a bacterial cell-wall lytic enzyme Biochim. Biophys. Acta 1960, 44 (0) 178-179
72. Brown, A. D.; Drummond, D. G.; North, R. J. The peripheral structures of Gram-negative bacteria: II. Membranes of bacilli and spheroplasts of a marine pseudomonad Biochim. Biophys. Acta 1962, 58 (3) 514-531
73. Pegg, A. E.; Michael, A. J. Spermine synthase Cell. Mol. Life Sci. 2010, 67 (1) 113-121
74. Joshi, G. S.; Spontak, J. S.; Klapper, D. G.; Richardson, A. R. Arginine catabolic mobile element encoded speG abrogates the unique hypersensitivity of Staphylococcus aureus to exogenous polyamines Mol. Microbiol. 2011, 82 (1) 9-20
75. Mashima, R.; Nakanishi-Ueda, T.; Yamamoto, Y. Simultaneous determination of methionine sulfoxide and methionine in blood plasma using gas chromatography-mass spectrometry Anal. Biochem. 2003, 313 (1) 28-33
76. Mailloux, R. J.; Singh, R.; Brewer, G.; Auger, C.; Lemire, J.; Appanna, V. D. α-Ketoglutarate Dehydrogenase and Glutamate Dehydrogenase Work in Tandem To Modulate the Antioxidant α-Ketoglutarate during Oxidative Stress in Pseudomonas fluorescens J. Bacteriol. 2009, 191 (12) 3804-3810
77. Mailloux, R. J.; Beriault, R.; Lemire, J.; Singh, R.; Chenier, D. R.; Hamel, R. D.; Appanna, V. D. The tricarboxylic acid cycle, an ancient metabolic network with a novel twist PLoS One 2007, 2 (8) e690