Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Subscribe

Logo for

Science 316 (5824): 593-597

Copyright © 2007 by the American Association for the Advancement of Science

Multiple High-Throughput Analyses Monitor the Response of E. coli to Perturbations

Nobuyoshi Ishii,1,2* Kenji Nakahigashi,1,2* Tomoya Baba,1,2,3* Martin Robert,1,2* Tomoyoshi Soga,1,2,6* Akio Kanai,1,2* Takashi Hirasawa,1,2* Miki Naba,1 Kenta Hirai,1 Aminul Hoque,1,2 Pei Yee Ho,5 Yuji Kakazu,1 Kaori Sugawara,1 Saori Igarashi,1 Satoshi Harada,1 Takeshi Masuda,1,2 Naoyuki Sugiyama,6 Takashi Togashi,1 Miki Hasegawa,1 Yuki Takai,1 Katsuyuki Yugi,1,2 Kazuharu Arakawa,1 Nayuta Iwata,1,2 Yoshihiro Toya,1,2 Yoichi Nakayama,1,2 Takaaki Nishioka,1,2,4 Kazuyuki Shimizu,1,2,5 Hirotada Mori,1,2,3 Masaru Tomita1,2,6{dagger}

Abstract: Analysis of cellular components at multiple levels of biological information can provide valuable functional insights. We performed multiple high-throughput measurements to study the response of Escherichia coli cells to genetic and environmental perturbations. Analysis of metabolic enzyme gene disruptants revealed unexpectedly small changes in messenger RNA and proteins for most disruptants. Overall, metabolite levels were also stable, reflecting the rerouting of fluxes in the metabolic network. In contrast, E. coli actively regulated enzyme levels to maintain a stable metabolic state in response to changes in growth rate. E. coli thus seems to use complementary strategies that result in a metabolic network robust against perturbations.

1 Institute for Advanced Biosciences, Keio University, Tsuruoka, Yamagata 997-0017, Japan.
2 Systems Biology Program, Graduate School of Media and Governance, Keio University, Fujisawa 252-8520, Japan.
3 Graduate School of Biological Sciences, Nara Institute of Science and Technology, Ikoma, Nara 630-0101, Japan.
4 Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan.
5 Department of Bioscience and Bioinformatics, Kyushu Institute of Technology, Iizuka, Fukuoka 820-8502, Japan.
6 Human Metabolome Technologies, Inc., Tsuruoka 997-0017, Japan.

* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: mt{at}sfc.keio.ac.jp


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Large-scale 13C-flux analysis reveals distinct transcriptional control of respiratory and fermentative metabolism in Escherichia coli.
B. R. B. Haverkorn van Rijsewijk, A. Nanchen, S. Nallet, R. J. Kleijn, and U. Sauer (2014)
Mol Syst Biol 7, 477
   Abstract »    Full Text »    PDF »
Absolute quantification of microbial proteomes at different states by directed mass spectrometry.
A. Schmidt, M. Beck, J. Malmstrom, H. Lam, M. Claassen, D. Campbell, and R. Aebersold (2014)
Mol Syst Biol 7, 510
   Abstract »    Full Text »    PDF »
Optimal regulatory strategies for metabolic pathways in Escherichia coli depending on protein costs.
F. Wessely, M. Bartl, R. Guthke, P. Li, S. Schuster, and C. Kaleta (2014)
Mol Syst Biol 7, 515
   Abstract »    Full Text »    PDF »
Systematic phenome analysis of Escherichia coli multiple-knockout mutants reveals hidden reactions in central carbon metabolism.
K. Nakahigashi, Y. Toya, N. Ishii, T. Soga, M. Hasegawa, H. Watanabe, Y. Takai, M. Honma, H. Mori, and M. Tomita (2014)
Mol Syst Biol 5, 306
   Abstract »    Full Text »    PDF »
Reconstruction of the yeast Snf1 kinase regulatory network reveals its role as a global energy regulator.
R. Usaite, M. C. Jewett, A. P. Oliveira, J. R. Yates III, L. Olsson, and J. Nielsen (2014)
Mol Syst Biol 5, 319
   Abstract »    Full Text »    PDF »
Tradeoff between enzyme and metabolite efficiency maintains metabolic homeostasis upon perturbations in enzyme capacity.
S.-M. Fendt, J. M. Buescher, F. Rudroff, P. Picotti, N. Zamboni, and U. Sauer (2014)
Mol Syst Biol 6, 356
   Abstract »    Full Text »    PDF »
Mass Spectrometry-based Workflow for Accurate Quantification of Escherichia coli Enzymes: How Proteomics Can Play a Key Role in Metabolic Engineering.
M. Trauchessec, M. Jaquinod, A. Bonvalot, V. Brun, C. Bruley, D. Ropers, H. de Jong, J. Garin, G. Bestel-Corre, and M. Ferro (2014)
Mol. Cell. Proteomics 13, 954-968
   Abstract »    Full Text »    PDF »
Prevalence of Virulence Genes Associated with Pathogenic Escherichia coli Strains Isolated from Domestically Harvested Rainwater during Low- and High-Rainfall Periods.
P. H. Dobrowsky, A. van Deventer, M. De Kwaadsteniet, T. Ndlovu, S. Khan, T. E. Cloete, and W. Khan (2014)
Appl. Envir. Microbiol. 80, 1633-1638
   Abstract »    Full Text »    PDF »
Dual role of transcription and transcript stability in the regulation of gene expression in Escherichia coli cells cultured on glucose at different growth rates.
T. Esquerre, S. Laguerre, C. Turlan, A. J. Carpousis, L. Girbal, and M. Cocaign-Bousquet (2014)
Nucleic Acids Res. 42, 2460-2472
   Abstract »    Full Text »    PDF »
Non-growing Rhodopseudomonas palustris Increases the Hydrogen Gas Yield from Acetate by Shifting from the Glyoxylate Shunt to the Tricarboxylic Acid Cycle.
J. B. McKinlay, Y. Oda, M. Ruhl, A. L. Posto, U. Sauer, and C. S. Harwood (2014)
J. Biol. Chem. 289, 1960-1970
   Abstract »    Full Text »    PDF »
Mapping Condition-Dependent Regulation of Lipid Metabolism in Saccharomyces cerevisiae.
M. C. Jewett, C. T. Workman, I. Nookaew, F. A. Pizarro, E. Agosin, L. I. Hellgren, and J. Nielsen (2013)
g3 3, 1979-1995
   Abstract »    Full Text »    PDF »
Metabolite Profiling to Characterize Disease-related Bacteria: GLUCONATE EXCRETION BY PSEUDOMONAS AERUGINOSA MUTANTS AND CLINICAL ISOLATES FROM CYSTIC FIBROSIS PATIENTS.
V. Behrends, T. J. Bell, M. Liebeke, A. Cordes-Blauert, S. N. Ashraf, C. Nair, J. E. A. Zlosnik, H. D. Williams, and J. G. Bundy (2013)
J. Biol. Chem. 288, 15098-15109
   Abstract »    Full Text »    PDF »
SS-mPMG and SS-GA: Tools for Finding Pathways and Dynamic Simulation of Metabolic Networks.
T. Katsuragi, N. Ono, K. Yasumoto, M. Altaf-Ul-Amin, M. Y. Hirai, K. Sriyudthsak, Y. Sawada, Y. Yamashita, Y. Chiba, H. Onouchi, et al. (2013)
Plant Cell Physiol. 54, 728-739
   Abstract »    Full Text »    PDF »
Physical Laws Shape Biology.
K. Selvarajoo and M. Tomita (2013)
Science 339, 646
   Full Text »    PDF »
Single-cell-type Proteomics: Toward a Holistic Understanding of Plant Function.
S. Dai and S. Chen (2012)
Mol. Cell. Proteomics 11, 1622-1630
   Abstract »    Full Text »    PDF »
Predicting Drug Targets and Biomarkers of Cancer via Genome-Scale Metabolic Modeling.
L. Jerby and E. Ruppin (2012)
Clin. Cancer Res. 18, 5572-5584
   Abstract »    Full Text »    PDF »
Coenzyme Q10 reverses mitochondrial dysfunction in atorvastatin-treated mice and increases exercise endurance.
A. Muraki, K. Miyashita, M. Mitsuishi, M. Tamaki, K. Tanaka, and H. Itoh (2012)
J Appl Physiol 113, 479-486
   Abstract »    Full Text »    PDF »
An integrated open framework for thermodynamics of reactions that combines accuracy and coverage.
E. Noor, A. Bar-Even, A. Flamholz, Y. Lubling, D. Davidi, and R. Milo (2012)
Bioinformatics 28, 2037-2044
   Abstract »    Full Text »    PDF »
Systems Biology, Metabolomics, and Cancer Metabolism.
M. Tomita and K. Kami (2012)
Science 336, 990-991
   Abstract »    Full Text »    PDF »
Multidimensional Optimality of Microbial Metabolism.
R. Schuetz, N. Zamboni, M. Zampieri, M. Heinemann, and U. Sauer (2012)
Science 336, 601-604
   Abstract »    Full Text »    PDF »
Reconfiguring Regulation.
G. Chalancon, K. Kruse, and M. M. Babu (2012)
Science 335, 1050-1051
   Abstract »    Full Text »    PDF »
Global Network Reorganization During Dynamic Adaptations of Bacillus subtilis Metabolism.
J. M. Buescher, W. Liebermeister, M. Jules, M. Uhr, J. Muntel, E. Botella, B. Hessling, R. J. Kleijn, L. Le Chat, F. Lecointe, et al. (2012)
Science 335, 1099-1103
   Abstract »    Full Text »    PDF »
influx_s: increasing numerical stability and precision for metabolic flux analysis in isotope labelling experiments.
S. Sokol, P. Millard, and J.-C. Portais (2012)
Bioinformatics 28, 687-693
   Abstract »    Full Text »    PDF »
Toward a Systems Biology Perspective on Enzyme Evolution.
S. D. Copley (2012)
J. Biol. Chem. 287, 3-10
   Abstract »    Full Text »    PDF »
High-Throughput Workflow for Monitoring and Mining Bioprocess Data and Its Application to Inferring the Physiological Response of Escherichia coli to Perturbations.
S. Heux, B. Philippe, and J.-C. Portais (2011)
Appl. Envir. Microbiol. 77, 7040-7049
   Abstract »    Full Text »    PDF »
Identification of metabolic network models from incomplete high-throughput datasets.
S. Berthoumieux, M. Brilli, H. de Jong, D. Kahn, and E. Cinquemani (2011)
Bioinformatics 27, i186-i195
   Abstract »    Full Text »    PDF »
Polynucleotide Phosphorylase Activity May Be Modulated by Metabolites in Escherichia coli.
S. Nurmohamed, H. A. Vincent, C. M. Titman, V. Chandran, M. R. Pears, D. Du, J. L. Griffin, A. J. Callaghan, and B. F. Luisi (2011)
J. Biol. Chem. 286, 14315-14323
   Abstract »    Full Text »    PDF »
Dispensability of Escherichia coli's latent pathways.
S. P. Cornelius, J. S. Lee, and A. E. Motter (2011)
PNAS 108, 3124-3129
   Abstract »    Full Text »    PDF »
OmicsAnalyzer: a Cytoscape plug-in suite for modeling omics data.
T. Xia, J. V. Hemert, and J. A. Dickerson (2010)
Bioinformatics 26, 2995-2996
   Abstract »    Full Text »    PDF »
Integrating quantitative proteomics and metabolomics with a genome-scale metabolic network model.
K. Yizhak, T. Benyamini, W. Liebermeister, E. Ruppin, and T. Shlomi (2010)
Bioinformatics 26, i255-i260
   Abstract »    Full Text »    PDF »
A systematic survey of in vivo obligate chaperonin-dependent substrates.
K. Fujiwara, Y. Ishihama, K. Nakahigashi, T. Soga, and H. Taguchi (2010)
EMBO J. 29, 1552-1564
   Abstract »    Full Text »    PDF »
Analysis of Metabolic Remodeling in Compensated Left Ventricular Hypertrophy and Heart Failure.
T. Kato, S. Niizuma, Y. Inuzuka, T. Kawashima, J. Okuda, Y. Tamaki, Y. Iwanaga, M. Narazaki, T. Matsuda, T. Soga, et al. (2010)
Circ Heart Fail 3, 420-430
   Abstract »    Full Text »    PDF »
Systems biology: opening new avenues in clinical research.
F. Molina, M. Dehmer, P. Perco, A. Graber, M. Girolami, G. Spasovski, J. P. Schanstra, and A. Vlahou (2010)
Nephrol. Dial. Transplant. 25, 1015-1018
   Full Text »    PDF »
Integrating multiple 'omics' analysis for microbial biology: application and methodologies.
W. Zhang, F. Li, and L. Nie (2010)
Microbiology 156, 287-301
   Abstract »    Full Text »    PDF »
Unbiased Quantitation of Escherichia coli Membrane Proteome Using Phase Transfer Surfactants.
T. Masuda, N. Saito, M. Tomita, and Y. Ishihama (2009)
Mol. Cell. Proteomics 8, 2770-2777
   Abstract »    Full Text »    PDF »
Phylogenetic Analysis of ADP-Glucose Pyrophosphorylase Subunits Reveals a Role of Subunit Interfaces in the Allosteric Properties of the Enzyme.
N. Georgelis, J. R. Shaw, and L. C. Hannah (2009)
Plant Physiology 151, 67-77
   Abstract »    Full Text »    PDF »
Genetic modification of flux for flux prediction of mutants.
Q. Zhao and H. Kurata (2009)
Bioinformatics 25, 1702-1708
   Abstract »    Full Text »    PDF »
A divide-and-conquer approach to analyze underdetermined biochemical models.
O. Kotte and M. Heinemann (2009)
Bioinformatics 25, 519-525
   Abstract »    Full Text »    PDF »
Continued Protein Synthesis at Low [ATP] and [GTP] Enables Cell Adaptation during Energy Limitation.
M. C. Jewett, M. L. Miller, Y. Chen, and J. R. Swartz (2009)
J. Bacteriol. 191, 1083-1091
   Abstract »    Full Text »    PDF »
Principles of transcriptional regulation and evolution of the metabolic system in E. coli.
A. S.N. Seshasayee, G. M. Fraser, M. M. Babu, and N. M. Luscombe (2009)
Genome Res. 19, 79-91
   Abstract »    Full Text »    PDF »
System estimation from metabolic time-series data.
G. Goel, I-C. Chou, and E. O. Voit (2008)
Bioinformatics 24, 2505-2511
   Abstract »    Full Text »    PDF »
Integration of Metabolomic and Proteomic Phenotypes: Analysis of Data Covariance Dissects Starch and RFO Metabolism from Low and High Temperature Compensation Response in Arabidopsis Thaliana.
S. Wienkoop, K. Morgenthal, F. Wolschin, M. Scholz, J. Selbig, and W. Weckwerth (2008)
Mol. Cell. Proteomics 7, 1725-1736
   Abstract »    Full Text »    PDF »
The PduX Enzyme of Salmonella enterica Is an L-Threonine Kinase Used for Coenzyme B12 Synthesis.
C. Fan and T. A. Bobik (2008)
J. Biol. Chem. 283, 11322-11329
   Abstract »    Full Text »    PDF »
Cyclic AMP-Dependent Catabolite Repression Is the Dominant Control Mechanism of Metabolic Fluxes under Glucose Limitation in Escherichia coli.
A. Nanchen, A. Schicker, O. Revelles, and U. Sauer (2008)
J. Bacteriol. 190, 2323-2330
   Abstract »    Full Text »    PDF »
Comparative transcriptomics reveals key gene expression differences between the human and bovine pathogens of the Mycobacterium tuberculosis complex.
P. Golby, K. A. Hatch, J. Bacon, R. Cooney, P. Riley, J. Allnutt, J. Hinds, J. Nunez, P. D. Marsh, R. G. Hewinson, et al. (2007)
Microbiology 153, 3323-3336
   Abstract »    Full Text »    PDF »
GENETICS: Getting Closer to the Whole Picture.
U. Sauer, M. Heinemann, and N. Zamboni (2007)
Science 316, 550-551
   Abstract »    Full Text »    PDF »

To Advertise     Find Products


Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882