Quantitative proteomic analysis reveals a simple strategy of global resource allocation in bacteria

被引:238
作者
Hui, Sheng [1 ]
Silverman, Josh M. [2 ,3 ]
Chen, Stephen S. [2 ,3 ]
Erickson, David W. [1 ]
Basan, Markus [1 ]
Wang, Jilong [1 ]
Hwa, Terence [1 ,4 ]
Williamson, James R. [2 ,3 ]
机构
[1] Univ Calif San Diego, Dept Phys, La Jolla, CA 92093 USA
[2] Scripps Res Inst, Dept Integrat Struct & Computat Biol, Skaggs Inst Chem Biol, La Jolla, CA 92037 USA
[3] Scripps Res Inst, Skaggs Inst Chem Biol, Dept Chem, La Jolla, CA 92037 USA
[4] Univ Calif San Diego, Div Biol Sci, Mol Biol Sect, La Jolla, CA 92093 USA
基金
美国国家科学基金会;
关键词
growth physiology; metabolic network; microbiology; quantitative proteomics; systems biology; ESCHERICHIA-COLI; MASS-SPECTROMETRY; ABSOLUTE QUANTIFICATION; PROTEIN-SYNTHESIS; GROWTH-RATE; GENE-EXPRESSION; BALANCED GROWTH; IN-VIVO; E; COIL; ABUNDANCE;
D O I
10.15252/msb.20145697
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
A central aim of cell biology was to understand the strategy of gene expression in response to the environment. Here, we study gene expression response to metabolic challenges in exponentially growing Escherichia coli using mass spectrometry. Despite enormous complexity in the details of the underlying regulatory network, we find that the proteome partitions into several coarse-grained sectors, with each sector's total mass abundance exhibiting positive or negative linear relations with the growth rate. The growth rate-dependent components of the proteome fractions comprise about half of the proteome by mass, and their mutual dependencies can be characterized by a simple flux model involving only two effective parameters. The success and apparent generality of this model arises from tight coordination between proteome partition and metabolism, suggesting a principle for resource allocation in proteome economy of the cell. This strategy of global gene regulation should serve as a basis for future studies on gene expression and constructing synthetic biological circuits. Coarse graining may be an effective approach to derive predictive phenomenological models for other 'omics' studies.
引用
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页数:15
相关论文
共 69 条
[1]   Mass spectrometry-based proteomics [J].
Aebersold, R ;
Mann, M .
NATURE, 2003, 422 (6928) :198-207
[2]   Predicting Cellular Growth from Gene Expression Signatures [J].
Airoldi, Edoardo M. ;
Huttenhower, Curtis ;
Gresham, David ;
Lu, Charles ;
Caudy, Amy A. ;
Dunham, Maitreya J. ;
Broach, James R. ;
Botstein, David ;
Troyanskaya, Olga G. .
PLOS COMPUTATIONAL BIOLOGY, 2009, 5 (01)
[3]   SELECTIVE DISADVANTAGE OF NON-FUNCTIONAL PROTEIN-SYNTHESIS IN ESCHERICHIA-COLI [J].
ANDREWS, KJ ;
HEGEMAN, GD .
JOURNAL OF MOLECULAR EVOLUTION, 1976, 8 (04) :317-328
[4]  
[Anonymous], 2011, PRINCIPLES MACROECON
[5]   Quantitative mass spectrometry in proteomics: a critical review [J].
Bantscheff, Marcus ;
Schirle, Markus ;
Sweetman, Gavain ;
Rick, Jens ;
Kuster, Bernhard .
ANALYTICAL AND BIOANALYTICAL CHEMISTRY, 2007, 389 (04) :1017-1031
[6]   EFFECTS OF FUSIDIC ACID ON GROWTH, RIBOSOME SYNTHESIS AND RNA-METABOLISM IN ESCHERICHIA-COLI [J].
BENNETT, PM ;
MAALOE, O .
JOURNAL OF MOLECULAR BIOLOGY, 1974, 90 (03) :541-561
[7]   Multiplexed absolute quantification in proteomics using artificial QCAT proteins of concatenated signature peptides [J].
Beynon, RJ ;
Doherty, MK ;
Pratt, JM ;
Gaskell, SJ .
NATURE METHODS, 2005, 2 (08) :587-589
[8]   The genome-wide transcriptional responses of Saccharomyces cerevisiae grown on glucose in aerobic chemostat cultures limited for carbon, nitrogen, phosphorus, or sulfur [J].
Boer, VM ;
de Winde, JH ;
Pronk, JT ;
Piper, MDW .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2003, 278 (05) :3265-3274
[9]   Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast [J].
Brauer, Matthew J. ;
Huttenhower, Curtis ;
Airoldi, Edoardo M. ;
Rosenstein, Rachel ;
Matese, John C. ;
Gresham, David ;
Boer, Viktor M. ;
Troyanskaya, Olga G. ;
Botstein, David .
MOLECULAR BIOLOGY OF THE CELL, 2008, 19 (01) :352-367
[10]  
Bremer H, 2009, ECOSAL ESCHERICHIA C, P1