Global dynamics of the Escherichia coli proteome and phosphoproteome during growth in minimal medium

Journal of Proteome Research

Volumn 12, Issue 6, 2013, Pages 2611-2621

  Soares, Nelson C ^a   Spät, Philipp ^a   Krug, Karsten ^a   MacEk, Boris ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

bacteria; Escherichia coli; growth; Orbitrap; phosphoproteomics

Indexed keywords

BACTERIAL PROTEIN; PHOSPHOPROTEIN; PROTEOME; SERINE; THREONINE; TYROSINE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CELL WALL; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIUM CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; ESCHERICHIA COLI; ISOTOPE LABELING; MOLECULAR DYNAMICS; MOLECULAR SIZE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84879401680     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr3011843     Document Type: Article

References (63)

1. Mijakovic, I.; Macek, B. Impact of phosphoproteomics on studies of bacterial physiology FEMS Microbiol. Rev. 2011, 36 (4) 877-92
2. Soufi, B.; Soares, N. C.; Ravikumar, V.; Macek, B. Proteomics reveals evidence of cross-talk between protein modifications in bacteria: focus on acetylation and phosphorylation Curr. Opin. Microbiol. 2012, 15 (3) 357-63
3. Macek, B.; Mijakovic, I. Site-specific analysis of bacterial phosphoproteomes Proteomics 2011, 11 (15) 3002-11
4. Kobir, A.; Shi, L.; Boskovic, A.; Grangeasse, C.; Franjevic, D.; Mijakovic, I. Protein phosphorylation in bacterial signal transduction Biochim. Biophys. Acta: Gen. Subj. 2011, 1810 (10) 989-94
5. Petranovic, D.; Michelsen, O.; Zahradka, K.; Silva, C.; Petranovic, M.; Jensen, P. R.; Mijakovic, I. Bacillus subtilis strain deficient for the protein-tyrosine kinase PtkA exhibits impaired DNA replication Mol. Microbiol. 2007, 63 (6) 1797-805
6. Manteca, A.; Ye, J.; Sánchez, J.; Jensen, O. N. Phosphoproteome analysis of Streptomyces development reveals extensive protein phosphorylation accompanying bacterial differentiation J. Proteome Res. 2011, 10 (12) 5481-92
7. Shah, I. M.; Laaberki, M.-H.; Popham, D. L.; Dworkin, J. A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments Cell 2008, 135 (3) 486-96
8. Klein, G.; Dartigalongue, C.; Raina, S. Phosphorylation-mediated regulation of heat shock response in Escherichia coli Mol. Microbiol. 2003, 48 (1) 269-85
9. Lacour, S.; Bechet, E.; Cozzone, A. J.; Mijakovic, I.; Grangeasse, C. Tyrosine phosphorylation of the UDP-Glucose dehydrogenase of Escherichia coli. Is at the crossroads of colanic acid synthesis and polymyxin resistance PLoS ONE 2008, 3 (8) e3053
10. Molle, V.; Kremer, L. Division and cell envelope regulation by Ser/Thr phosphorylation: Mycobacterium shows the way Mol. Microbiol. 2010, 75 (5) 1064-77
11. Ge, R.; Shan, W. Bacterial phosphoproteomic analysis reveals the correlation between protein phosphorylation and bacterial pathogenicity Genomics, Proteomics Bioinform. 2011, 9 (4-5) 119-27
12. Morona, J. K.; Miller, D. C.; Morona, R.; Paton, J. C. The effect that mutations in the conserved capsular polysaccharide biosynthesis genes cpsA, cpsB, and cpsD have on virulence of Streptococcus pneumoniae J. Infect. Dis. 2004, 189 (10) 1905-13
13. Schumacher, M. A.; Piro, K. M.; Xu, W.; Hansen, S.; Lewis, K.; Brennan, R. G. Molecular mechanisms of HipA-mediated multidrug tolerance and Its neutralization by HipB Science 2009, 323 (5912) 396-401
14. Macek, B.; Mijakovic, I.; Olsen, J. V.; Gnad, F.; Kumar, C.; Jensen, P. R.; Mann, M. The Serine/Threonine/Tyrosine phosphoproteome of the model bacterium Bacillus subtilis Mol. Cell. Proteomics 2007, 6 (4) 697-707
15. Macek, B.; Gnad, F.; Soufi, B.; Kumar, C.; Olsen, J. V.; Mijakovic, I.; Mann, M. Phosphoproteome analysis of E. coli reveals evolutionary conservation of bacterial Ser/Thr/Tyr phosphorylation Mol. Cell. Proteomics 2008, 7 (2) 299-307
16. Schmidl, S. R.; Gronau, K.; Pietack, N.; Hecker, M.; Becher, D.; Stülke, J. The phosphoproteome of the minimal bacterium Mycoplasma pneumoniae Mol. Cell. Proteomics 2010, 9 (6) 1228-42
17. Ravichandran, A.; Sugiyama, N.; Tomita, M.; Swarup, S.; Ishihama, Y. Ser/Thr/Tyr phosphoproteome analysis of pathogenic and non-pathogenic Pseudomonas species Proteomics 2009, 9 (10) 2764-75
18. Parker, J. L.; Jones, A. M. E.; Serazetdinova, L.; Saalbach, G.; Bibb, M. J.; Naldrett, M. J. Analysis of the phosphoproteome of the multicellular bacterium Streptomyces coelicolor A3(2) by protein/peptide fractionation, phosphopeptide enrichment and high-accuracy mass spectrometry Proteomics 2010, 10 (13) 2486-97
19. Soufi, B.; Gnad, F.; Jensen, P. R.; Petranovic, D.; Mann, M.; Mijakovic, I.; Macek, B. The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins Proteomics 2008, 8 (17) 3486-93
20. Ge, R.; Sun, X.; Xiao, C.; Yin, X.; Shan, W.; Chen, Z.; He, Q.-Y. Phosphoproteome analysis of the pathogenic bacterium Helicobacter pylori reveals over-representation of tyrosine phosphorylation and multiply phosphorylated proteins Proteomics 2011, 11 (8) 1449-61
21. Prisic, S.; Dankwa, S.; Schwartz, D.; Chou, M. F.; Locasale, J. W.; Kang, C.-M.; Bemis, G.; Church, G. M.; Steen, H.; Husson, R. N. Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases Proc. Natl. Acad. Sci. 2010, 107 (16) 7521-6
22. Hempel, K.; Pané-Farré, J.; Otto, A.; Sievers, S.; Hecker, M.; Becher, D. r. Quantitative cell surface proteome profiling for SigB-dependent protein expression in the human pathogen Staphylococcus aureus via biotinylation approach J. Proteome Res. 2010, 9 (3) 1579-90
23. Ong, S.-E.; Blagoev, B.; Kratchmarova, I.; Kristensen, D. B.; Steen, H.; Pandey, A.; Mann, M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol. Cell. Proteomics 2002, 1 (5) 376-86
24. Soufi, B.; Kumar, C.; Gnad, F.; Mann, M.; Mijakovic, I.; Macek, B. Stable isotope labeling by amino acids in cell culture (SILAC) applied to quantitative proteomics of Bacillus subtilis J. Proteome Res. 2010, 9 (7) 3638-46
25. Macek, B.; Mann, M.; Olsen, J. V. Global and site-specific quantitative phosphoproteomics: principles and applications Annu. Rev. Pharmacol. Toxicol. 2009, 49, 199-221
26. Schreiber, T. B.; Mäusbacher, N.; Breitkopf, S. B.; Grundner-Culemann, K.; Daub, H. Quantitative phosphoproteomics-an emerging key technology in signal-transduction research Proteomics 2008, 8 (21) 4416-32
27. Olsen, J. V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks Cell 2006, 127 (3) 635-48
28. Pan, C.; Gnad, F.; Olsen, J. V.; Mann, M. Quantitative phosphoproteome analysis of a mouse liver cell line reveals specificity of phosphatase inhibitors Proteomics 2008, 8 (21) 4534-46
29. Nystrom, T. Stationary-phase physiology Annu. Rev. Microbiol. 2004, 58 (1) 161
30. Hengge-Aronis, R. Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase Microbiology and Molecular Biology Reviews 2002, 66 (3) 373-95
31. Jers, C.; Kobir, A.; Søndergaard, E. O.; Jensen, P. R.; Mijakovic, I. Bacillus subtilis two-component system sensory kinase DegS is regulated by Serine phosphorylation in its input domain PLoS ONE 2011, 6 (2) e14653
32. Bernhardt, J.; Weibezahn, J.; Scharf, C.; Hecker, M. Bacillus subtilis during feast and famine: visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis Genome Res. 2003, 13 (2) 224-37
33. Lee, K.-J.; Bae, S.-M.; Lee, M.-R.; Yeon, S.-M.; Lee, Y.-H.; Kim, K.-S. Proteomic analysis of growth phase-dependent proteins of Streptococcus pneumoniae Proteomics 2006, 6 (4) 1274-82
34. Soares, N. C.; Cabral, M. P.; Gayoso, C.; Mallo, S.; Rodriguez-Velo, P.; Fernández-Moreira, E.; Bou, G. Associating growth-phase-related changes in the proteome of Acinetobacter baumannii with increased resistance to oxidative stress J. Proteome Res. 2010, 9 (4) 1951-64
35. Monod, J. The growth of bacterial cultures Annu. Rev. Microbiol. 1949, 3 (1) 371-94
36. Ishihama, Y.; Rappsilber, J.; Mann, M. Modular stop and go extraction tips with stacked disks for parallel and multidimensional peptide fractionation in proteomics J. Proteome Res. 2006, 5 (4) 988-94
37. Franz-Wachtel, M.; Eisler, S. A.; Krug, K.; Wahl, S.; Carpy, A.; Nordheim, A.; Pfizenmaier, K.; Hausser, A.; Macek, B. Global detection of protein kinase D-dependent phosphorylation events in nocodazole-treated human cells Mol. Cell. Proteomics 2012, 11 (5) 160-70
38. Olsen, J. V.; de Godoy, L. M. F.; Li, G.; Macek, B.; Mortensen, P.; Pesch, R.; Makarov, A.; Lange, O.; Horning, S.; Mann, M. Parts per million mass cccuracy on an orbitrap mass spectrometer via lock mass injection into a C-trap Mol. Cell. Proteomics 2005, 4 (12) 2010-21
39. Cox, J.; Matic, I.; Hilger, M.; Nagaraj, N.; Selbach, M.; Olsen, J. V.; Mann, M. A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics Nat. Protocols 2009, 4 (5) 698-705
40. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing J. R. Stat. Soc. Ser. B: Methodol. 1995, 57 (1) 289-300
41. Olsen, J. V.; Vermeulen, M.; Santamaria, A.; Kumar, C.; Miller, M. L.; Jensen, L. J.; Gnad, F.; Cox, J.; Jensen, T. S.; Nigg, E. A.; Brunak, S.; Mann, M. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis Sci. Signal. 2010, 3 (104) ra3
42. Larance, M.; Bailly, A. P.; Pourkarimi, E.; Hay, R. T.; Buchanan, G.; Coulthurst, S.; Xirodimas, D. P.; Gartner, A.; Lamond, A. I. Stable-isotope labeling with amino acids in nematodes Nat. Methods 2011, 8 (10) 849-51
43. Matic, I.; Jaffray, E. G.; Oxenham, S. K.; Groves, M. J.; Barratt, C. L. R.; Tauro, S.; Stanley-Wall, N. R.; Hay, R. T. Absolute SILAC-compatible expression strain allows Sumo-2 copy number determination in clinical samples J. Proteome Res. 2011, 10 (10) 4869-75
44. Neher, S. B.; Villén, J.; Oakes, E. C.; Bakalarski, C. E.; Sauer, R. T.; Gygi, S. P.; Baker, T. A. Proteomic profiling of ClpXP substrates after DNA damage reveals extensive instability within SOS regulon Mol. Cell 2006, 22 (2) 193-204
45. Waanders, L. F.; Hankes, S.; Mann, M. Top-down quantitationand characterization of SILAC-labeled proteins J. Am. Soc. Mass Spectrom. 2007, 18 (11) 2058-64
46. Zeiler, M.; Straube, W. L.; Lundberg, E.; Uhlen, M.; Mann, M. A Protein epitope signature tag (PrEST) library allows SILAC-based absolute quantification and multiplexed determination of protein copy numbers in cell lines Mol. Cell. Proteomics 2012, 11 (3 O111.009613
47. Kuroda, A.; Nomura, K.; Ohtomo, R.; Kato, J.; Ikeda, T.; Takiguchi, N.; Ohtake, H.; Kornberg, A. Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli Science 2001, 293 (5530) 705-8
48. Ishihama, A. Functional modulation of Escherichia coli RNA polymerase Annu. Rev. Microbiol. 2000, 54 (1) 499-518
49. Charoenwong, D.; Andrews, S.; Mackey, B. Role of rpoS in the development of cell envelope resilience and pressure resistance in stationary-phase Escherichia coli Appl. Environ. Microbiol. 2011, 77 (15) 5220-9
50. Battesti, A.; Majdalani, N.; Gottesman, S. The RpoS-mediated general stress response in Escherichia coli * Annu. Rev. Microbiol. 2011, 65 (1) 189-213
51. Dong, T.; Schellhorn, H. Control of RpoS in global gene expression of Escherichia coli in minimal media Molecular Genetics and Genomics 2009, 281 (1) 19-33
52. Tao, H.; Bausch, C.; Richmond, C.; Blattner, F. R.; Conway, T. Functional Genomics: Expression analysis of Escherichia coli growing on minimal and rich media J. Bacteriol. 1999, 181 (20) 6425-40
53. Schultz, J. E.; Matin, A. Molecular and functional characterization of a carbon starvation gene of Escherichia coli J. Mol. Biol. 1991, 218 (1) 129-40
54. Marschall, C.; Labrousse, V.; Kreimer, M.; Weichart, D.; Kolb, A.; Hengge-Aronis, R. Molecular analysis of the regulation of csiD, a carbon starvation-inducible gene in Escherichia coli that is exclusively dependent on σS and requires activation by cAMP-CRP J. Mol. Biol. 1998, 276 (2) 339-53
55. Lutticke, C.; Hauske, P.; Lewandrowski, U.; Sickmann, A.; Kaiser, M.; Ehrmann, M. E. coli LoiP (YggG), a metalloprotease hydrolyzing Phe-Phe bonds Mol. BioSyst. 2012, 8 (6) 1775-82
56. Huang, Y.; Zhang, B.; Dong, K.; Zhang, X.; Hou, L.; Wang, T.; Chen, N.; Chen, S. Up-regulation of yggG promotes the survival of Escherichia coli cells containing Era-1 mutant protein FEMS Microbiol. Lett. 2007, 275 (1) 8-15
57. Jung, J. U.; Gutierrez, C.; Martin, F.; Ardourel, M.; Villarejo, M. Transcription of osmB, a gene encoding an Escherichia coli lipoprotein, is regulated by dual signals. Osmotic stress and stationary phase J. Biol. Chem. 1990, 265 (18) 10574-81
58. Jung, J. U.; Gutierrez, C.; Villarejo, M. R. Sequence of an osmotically inducible lipoprotein gene J. Bacteriol. 1989, 171 (1) 511-20
59. Soung, G. Y.; Miller, J. L.; Koc, H.; Koc, E. C. Comprehensive analysis of phosphorylated proteins of Escherichia coli ribosomes J. Proteome Res. 2009, 8 (7) 3390-402
60. Zhang, Y.; Yu, N.-J.; Spremulli, L. L. Mutational analysis of the roles of residues in Escherichia coli elongation factor Ts in the interaction with Elongation Factor Tu J. Biol. Chem. 1998, 273 (8) 4556-62
61. Sajid, A.; Arora, G.; Gupta, M.; Singhal, A.; Chakraborty, K.; Nandicoori, V. K.; Singh, Y. Interaction of Mycobacterium tuberculosis elongation factor Tu with GTP is regulated by phosphorylation J. Bacteriol. 2011, 193 (19) 5347-58
62. Hansen, A.-M.; Qiu, Y.; Yeh, N.; Blattner, F. R.; Durfee, T.; Jin, D. J. SspA is required for acid resistance in stationary phase by downregulation of H-NS in Escherichia coli Mol. Microbiol. 2005, 56 (3) 719-34
63. Archambaud, C.; Nahori, M. A.; Pizarro-Cerda, J.; Cossart, P.; Dussurget, O. Control of Listeria superoxide dismutase by phosphorylation J. Biol. Chem. 2006, 281 (42) 31812-22