Highly precise quantification of protein molecules per cell during stress and starvation responses in bacillus subtilis

Molecular and Cellular Proteomics

Volumn 13, Issue 9, 2014, Pages 2260-2276

  Maaß, Sandra ^a   Wachlin, Gerhild ^a   Bernhardt, Jörg ^a   Eymann, Christine ^a   Fromion, Vincent ^b   Riedel, Katharina ^a   Becher, Dörte ^a   Hecker, Michael ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BRANCHED CHAIN AMINO ACID; CHAPERONE; CYTOPLASM PROTEIN; GLUCOSE; MISMATCH REPAIR PROTEIN;

AMINO ACID SYNTHESIS; ANIMAL CELL; ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GROWTH; CARBON METABOLISM; CELL COUNT; CELL DISRUPTION; CELL GROWTH; DOWN REGULATION; GLUCOSE STARVATION; HEAT STRESS; LIMIT OF DETECTION; LIMIT OF QUANTITATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPTICAL DENSITY; PROTEIN CONTENT; PROTEIN DEPLETION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; STARVATION; STOICHIOMETRY; ADAPTATION; HEAT; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

BACILLUS SUBTILIS;

ADAPTATION, PHYSIOLOGICAL; BACILLUS SUBTILIS; BACTERIAL PROTEINS; GLUCOSE; HOT TEMPERATURE; STRESS, PHYSIOLOGICAL;

EID: 84907225985     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.035741     Document Type: Article

References (56)

1. Aebersold, R. (2005) Molecular Systems Biology: a new journal for a new biology? Mol. Syst. Biol. 1, 2005.0005
2. Souchelnytskyi, S. (2005) Bridging proteomics and systems biology: What are the roads to be traveled? Proteomics 5, 4123-4137
3. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003) Global analysis of protein expression in yeast. Annu. Rev. Plant Physiol. Plant Mol. Biol. 41, 55-75
4. Ishihama, Y., Schmidt, T., Rappsilber, J., Mann, M., Hartl, F. U., Kerner, M. J., and Frishman, D. (2008) Protein abundance profiling of the Escherichia coli cytosol. BMC genomics 9, 102
5. Malmström, J., Beck, M., Schmidt, A., Lange, V., Deutsch, E. W., and Aebersold, R. (2009) Proteome-wide cellular protein concentrations of the human pathogen Leptospira interrogans. Nature 460, 762-765
6. Maass, S., Sievers, S., Zühlke, D., Kuzinski, J., Sappa, P. K., Muntel, J., Hessling, B., Bernhardt, J., Sietmann, R., Völker, U., Hecker, M., and Becher, D. (2011) Efficient, global-scale quantification of absolute protein amounts by integration of targeted mass spectrometry and two-dimensional gel-based proteomics. Anal. Chem. 83, 2677-2684
7. Baudouin-Cornu, P., Lagniel, G., Chédin, S., and Labarre, J. (2009) Development of a new method for absolute protein quantification on twodimensional gels. Proteomics 9, 4606-4615
8. Lu, P., Vogel, C., Wang, R., Yao, X., and Marcotte, E. M. (2007) Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat. Biotechnol. 25, 117-124
9. Schmidt, A., Beck, M., Malmström, J., Lam, H., Claassen, M., Campbell, D., and Aebersold, R. (2011) Absolute quantification of microbial proteomes at different states by directed mass spectrometry. Mol. Syst. Biol. 7, 510
10. Bernhardt, J., Weibezahn, J., Scharf, C., and Hecker, M. (2003) Bacillus subtilis during feast and famine: visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis. Genome Res. 13, 224-237
11. Hecker, M., and Völker, U. (2001) General stress response of Bacillus subtilis and other bacteria. Adv. Microb. Physiol. 44, 35-91
12. Price, C. W., Fawcett, P., Cérémonie, H., Su, N., Murphy, C. K., and Youngman, P. (2001) Genome-wide analysis of the general stress response in Bacillus subtilis. Mol. Microbiol. 41, 757-774
13. Yang, X., Kang, C. M., Brody, M. S., and Price, C. W. (1996) Opposing pairs of serine protein kinases and phosphatases transmit signals of environmental stress to activate a bacterial transcription factor. Genes Dev. 10, 2265-2275
14. Voelker, U., Voelker, A., Maul, B., Hecker, M., Dufour, A., and Haldenwang, W. G. (1995) Separate mechanisms activate sigma B of Bacillus subtilis in response to environmental and metabolic stresses. J. Bacteriol. 177, 3771-3780
15. Vijay, K., Brody, M. S., Fredlund, E., and Price, C. W. (2000) A PP2C phosphatase containing a PAS domain is required to convey signals of energy stress to the sigmaB transcription factor of Bacillus subtilis. Mol. Microbiol. 35, 180-188
16. Eymann, C., Homuth, G., Scharf, C., and Hecker, M. (2002) Bacillus subtilis functional genomics: global characterization of the stringent response by proteome and transcriptome analysis. J. Bacteriol. 184, 2500-2520
17. Koburger, T., Weibezahn, J., Bernhardt, J., Homuth, G., and Hecker, M. (2005) Genome-wide mRNA profiling in glucose starved Bacillus subtilis cells. Mol. Genet. Genomics 274, 1-12
18. Otto, A., Bernhardt, J., Meyer, H., Schaffer, M., Herbst, F.-A., Siebourg, J., Mäder, U., Lalk, M., Hecker, M., and Becher, D. (2010) Systems-wide temporal proteomic profiling in glucose-starved Bacillus subtilis. Nat. Commun. 1, 137
19. Gerth, U., Kock, H., Kusters, I., Michalik, S., Switzer, R. L., and Hecker, M. (2008) Clp-dependent proteolysis down-regulates central metabolic pathways in glucose-starved Bacillus subtilis. J. Bacteriol. 190, 321-331
20. Schulz, A., and Schumann, W. (1996) hrcA, the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J. Bacteriol. 178, 1088-1093
21. Derré, I., Rapoport, G., and Msadek, T. (1999) CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria. Mol. Microbiol. 31, 117-131
22. Derré, I., Rapoport, G., Devine, K., Rose, M., and Msadek, T. (1999) ClpE, a novel type of HSP100 ATPase, is part of the CtsR heat shock regulon of Bacillus subtilis. Mol. Microbiol. 32, 581-593
23. Krüger, E., and Hecker, M. (1998) The first gene of the Bacillus subtilis clpC operon, ctsR, encodes a negative regulator of its own operon and other class III heat shock genes. J. Bacteriol. 180, 6681-6688
24. Schumann, W. (2003) The Bacillus subtilis heat shock stimulon. Cell Stress Chaperones 8, 207-217
25. Deuerling, E., Mogk, A., Richter, C., Purucker, M., and Schumann, W. (1997) The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol. Microbiol. 23, 921-933
26. Gerth, U., Krüger, E., Derré, I., Msadek, T., and Hecker, M. (1998) Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance. Mol. Microbiol. 28, 787-802
27. Schumann, W., Hecker, M., and Msadek, T. (2002) in Bacillus subtilis and its Closest Relatives: From Genes to Cells, eds Sonenshein AL, Losick R, Hoch JA (ASM Press, Washington), pp 359-368.
28. Riethdorf, S., Völker, U., Gerth, U., Winkler, A., Engelmann, S., and Hecker, M. (1994) Cloning, nucleotide sequence, and expression of the Bacillus subtilis lon gene. J. Bacteriol. 176, 6518-6527
29. Antelmann, H., Engelmann, S., Schmid, R., and Hecker, M. (1996) General and oxidative stress responses in Bacillus subtilis: cloning, expression, and mutation of the alkyl hydroperoxide reductase operon. J. Bacteriol. 178, 6571-6578
30. Moch, C., Schrögel, O., and Allmansberger, R. (2000) Transcription of the nfrA-ywcH operon from Bacillus subtilis is specifically induced in response to heat. J. Bacteriol. 182, 4384-4393
31. Zuber, U., Drzewiecki, K., and Hecker, M. (2001) Putative sigma factor SigI (YkoZ) of Bacillus subtilis is induced by heat shock. J. Bacteriol. 183, 1472-1475
32. Jules, M., Le Chat, L., Aymerich, S., and Le Coq, D. (2009) The Bacillus subtilis ywjI (glpX) Gene Encodes a Class II Fructose-1,6-Bisphosphatase, Functionally Equivalent to the Class III Fbp Enzyme. J. Bacteriol. 191, 3168-3171
33. Stülke, J., Hanschke, R., and Hecker, M. (1993) Temporal activation of beta-glucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J. Gen. Microbiol. 139, 2041-2045
34. Starcher, B. (2001) A ninhydrin-based assay to quantitate the total protein content of tissue samples. Anal. Biochem. 292, 125-129
35. Büttner, K., Bernhardt, J., Scharf, C., Schmid, R., Mäder, U., Eymann, C., Antelmann, H., Völker, A., Völker, U., and Hecker, M. (2001) A comprehensive two-dimensional map of cytosolic proteins of Bacillus subtilis. Electrophoresis 22, 2908-2935
36. Sahai, H., and Ojeda, M. M. (2004) in Analysis of Variance for Random Models, Volume 2: Unbalanced Data: Theory, Methods, Applications, and Data Analysis (Springer), pp 331-342
37. Pettit, F. H., Hamilton, L., Munk, P., Namihira, G., Eley, M. H., Willms, C. R., and Reed, L. J. (1973) Alpha-keto acid dehydrogenase complexes. XIX. Subunit structure of the Escherichia coli alpha-ketoglutarate dehydrogenase complex. J. Biol. Chem. 248, 5282-5290
38. Meyer, F. M., Gerwig, J., Hammer, E., Herzberg, C., Commichau, F. M., Völker, U., and Stülke, J. (2011) Physical interactions between tricarboxylic acid cycle enzymes in Bacillus subtilis: evidence for a metabolon. Metab. Eng. 13, 18-27
39. Ludwig, H., Homuth, G., Schmalisch, M., Dyka, F. M., Hecker, M., and Stülke, J. (2001) Transcription of glycolytic genes and operons in Bacillus subtilis: evidence for the presence of multiple levels of control of the gapA operon. Mol. Microbiol. 41, 409-422
40. Tobisch, S., Zühlke, D., Bernhardt, J., Stülke, J., and Hecker, M. (1999) Role of CcpA in regulation of the central pathways of carbon catabolism in Bacillus subtilis. J. Bacteriol. 181, 6996-7004
41. Fillinger, S., Boschi-Muller, S., Azza, S., Dervyn, E., Branlant, G., and Aymerich, S. (2000) Two glyceraldehyde-3-phosphate dehydrogenases with opposite physiological roles in a nonphotosynthetic bacterium. J. Biol. Chem. 275, 14031-14037
42. Bar-Even, A., Noor, E., Savir, Y., Liebermeister, W., Davidi, D., Tawfik, D. S., and Milo, R. (2011) The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50, 4402-4410
43. Bernhardt, J., Völker, U., Völker, A., Antelmann, H., Schmid, R., Mach, H., and Hecker, M. (1997) Specific and general stress proteins in Bacillus subtilis-a two-dimensional protein electrophoresis study. Microbiology 143, 999-1017
44. Helmann, J. D., Wu, M. F., Kobel, P. A., Gamo, F. J., Wilson, M., Morshedi, M. M., Navre, M., and Paddon, C. (2001) Global transcriptional response of Bacillus subtilis to heat shock. J. Bacteriol. 183, 7318-7328
45. Reder, A., Höper, D., Gerth, U., and Hecker, M. (2012) Contributions of individual B-dependent general stress genes to oxidative stress resistance of Bacillus subtilis. J. Bacteriol. 194, 3601-3610
46. Höper, D., Völker, U., and Hecker, M. (2005) Comprehensive characterization of the contribution of individual SigB-dependent general stress genes to stress resistance of Bacillus subtilis. J. Bacteriol. 187, 2810-2826
47. Gerth, U., Kirstein, J., Mostertz, J., Waldminghaus, T., Miethke, M., Kock, H., and Hecker, M. (2004) Fine-Tuning in Regulation of Clp Protein Content in Bacillus subtilis. J. Bacteriol. 186, 179-191
48. Zhou, M., Boekhorst, J., Francke, C., and Siezen, R. J. (2008) LocateP: genome-scale subcellular-location predictor for bacterial proteins. BMC Bioinf. 9, 173
49. Becher, D., Hempel, K., Sievers, S., Zühlke, D., Pané-Farré, J., Otto, A., Fuchs, S., Albrecht, D., Bernhardt, J., Engelmann, S., Völker, U., van Dijl, J. M., and Hecker, M. (2009) A proteomic view of an important human pathogen-towards the quantification of the entire Staphylococcus aureus proteome. PLoS ONE 4, e8176
50. Wolff, S., Otto, A., Albrecht, D., Zeng, J. S., Büttner, K., Glückmann, M., Hecker, M., and Becher, D. (2006) Gel-free and gel-based proteomics in Bacillus subtilis: a comparative study. Mol. Cell. Proteomics 5, 1183-1192
51. Muntel, J., Fromion, V., Goelzer, A., Maa, S., Mäder, U., Büttner, K., Hecker, M., and Becher, D. (2014) Comprehensive absolute quantification of the cytosolic proteome of Bacillus subtilis by data independent, parallel fragmentation in Liquid Chromatography/Mass Spectrometry (LC/MSE). Mol. Cell. Proteomics 13, 1008-1019
52. Hahne, H., Mäder, U., Otto, A., Bonn, F., Steil, L., Bremer, E., Hecker, M., and Becher, D. (2010) A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation. J. Bacteriol. 192, 870-882
53. Reder, A., Höper, D., Weinberg, C., Gerth, U., Fraunholz, M., and Hecker, M. (2008) The Spx paralogue MgsR (YqgZ) controls a subregulon within the general stress response of Bacillus subtilis. Mol. Microbiol. 69, 1104-1120
54. Schulz, A., Schwab, S., Homuth, G., Versteeg, S., and Schumann, W. (1997) The htpG gene of Bacillus subtilis belongs to class III heat shock genes and is under negative control. J. Bacteriol. 179, 3103-3109
55. Newman, J. R. S., Ghaemmaghami, S., Ihmels, J., Breslow, D. K., Noble, M., DeRisi, J. L., and Weissman, J. S. (2006) Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441, 840-846
56. Masuda, T., Saito, N., Tomita, M., and Ishihama, Y. (2009) Unbiased quantitation of Escherichia coli membrane proteome using phase-transfer surfactants. Mol. Cell. Proteomics 8, 2770-2777