Regulation and control of metabolic fluxes in microbes

Current Opinion in Biotechnology

Volumn 22, Issue 4, 2011, Pages 566-575

  Gerosa, Luca ^a,b   Sauer, Uwe ^a  

^a ETH ZURICH   (Switzerland)

^b Life Science Zurich   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME PHOSPHORYLATION; FEEDBACK SIGNAL; FUNCTIONAL RELEVANCE; KNOWLEDGE GAPS; METABOLIC FLUX; MICROBIAL METABOLISM; POST-TRANSLATIONAL MODIFICATIONS; REGULATION AND CONTROL; REGULATORY CIRCUITS; REGULATORY MECHANISM; REGULATORY NETWORK; SYSTEMATIC ANALYSIS;

ACETYLATION; CELL PROLIFERATION; ELECTRIC NETWORK TOPOLOGY; PHOSPHORYLATION; PHYSIOLOGY; TOPOLOGY;

METABOLISM;

BACTERIAL PROTEIN;

ACETYLATION; BACTERIUM; CELL DIFFERENTIATION; CELL PROLIFERATION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; EVOLUTION; FEEDBACK SYSTEM; METABOLIC REGULATION; METABOLITE; MICROBIAL METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; YEAST;

BACTERIA; BACTERIAL PROTEINS; FUNGAL PROTEINS; FUNGI; METABOLIC NETWORKS AND PATHWAYS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION;

EID: 79960964285     PISSN: 09581669     EISSN: 18790429     Source Type: Journal    
DOI: 10.1016/j.copbio.2011.04.016     Document Type: Review

References (87)

1. Sauer U. Metabolic networks in motion: 13C-based flux analysis. Molecular Systems Biology 2006, 2:62.
2. Oberhardt M.A., Palsson B., Papin J.A. Applications of genome-scale metabolic reconstructions. Molecular Systems Biology 2009, 5:320.
3. Reaves M.L., Rabinowitz J.D. Metabolomics in systems microbiology. Current Opinion in Biotechnology 2011, 22:17-25.
4. Zamboni N., Sauer U. Novel biological insights through metabolomics and 13C-flux analysis. Current Opinion in Microbiology 2009, 12:553-558.
5. Ray L.B. Metabolism. Metabolism is not boring. Introduction. Science (New York, NY) 2010, 330:1337.
6. Heinemann M., Sauer U. Systems biology of microbial metabolism. Current Opinion in Microbiology 2010, 13:337-343.
7. Cho B.-K., Zengler K., Qiu Y., Park Y.S., Knight E.M., Barrett C.L., Gao Y., Palsson B. The transcription unit architecture of the Escherichia coli genome. Nature Biotechnology 2009, 27:1043-1049.
8. Bodenmiller B., Wanka S., Kraft C., Urban J., Campbell D., Pedrioli P.G., Gerrits B., Picotti P., Lam H., Vitek O., et al. Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast. Science Signaling 2010, 3:rs4-rs14.
9. Keseler I.M., Bonavides-Martínez C., Collado-Vides J., Gama-Castro S., Gunsalus R.P., Johnson D.A., Krummenacker M., Nolan L.M., Paley S., Paulsen I.T., et al. EcoCyc: a comprehensive view of Escherichia coli biology. Nucleic Acids Research 2009, 37:D464-D470.
10. Shimada T., Yamamoto K., Ishihama A. Novel members of the Cra regulon involved in carbon metabolism in Escherichia coli. Journal of Bacteriology 2010, 193:649-659.
11. Cho B.-K., Barrett C.L., Knight E.M., Park Y.S., Palsson B. Genome-scale reconstruction of the Lrp regulatory network in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:19462-19467.
12. Seshasayee A.S.N., Fraser G.M., Babu M.M., Luscombe N.M. Principles of transcriptional regulation and evolution of the metabolic system in E. coli. Genome Research 2009, 19:79-91.
13. Janga S.C., Salgado H., Martínez-Antonio A. Transcriptional regulation shapes the organization of genes on bacterial chromosomes. Nucleic Acids Research 2009, 37:3680-3688.
14. Mendoza-Vargas A., Olvera L., Olvera M., Grande R., Vega-Alvarado L., Taboada B., Jimenez-Jacinto V., Salgado H., Juárez K., Contreras-Moreira B., et al. Genome-wide identification of transcription start sites, promoters and transcription factor binding sites in E. coli. PLoS ONE 2009, 4:e7526.
15. Naville M., Gautheret D. Transcription attenuation in bacteria: theme and variations. Briefings in Functional Genomics 2010, 9:178.
16. Durand S., Storz G. Reprogramming of anaerobic metabolism by the FnrS small RNA. Molecular Microbiology 2010, 75:1215-1231.
17. Pietack N., Becher D., Schmidl S.R., Saier M.H., Hecker M., Commichau F.M., Stülke J. In vitro phosphorylation of key metabolic enzymes from Bacillus subtilis: PrkC phosphorylates enzymes from different branches of basic metabolism. Journal of Molecular Microbiology and Biotechnology 2010, 18:129-140.
18. Gnad F., Forner F., Zielinska D.F., Birney E., Gunawardena J., Mann M. Evolutionary constraints of phosphorylation in eukaryotes, prokaryotes, and mitochondria. Molecular & Cellular Proteomics: MCP 2010, 9:2642-2653.
19. Schmidl S.R., Gronau K., Pietack N., Hecker M., Becher D., Stülke J. The phosphoproteome of the minimal bacterium Mycoplasma pneumoniae: analysis of the complete known Ser/Thr kinome suggests the existence of novel kinases. Molecular & Cellular Proteomics: MCP 2010, 9:1228-1242.
20. Sun X., Ge F., Xiao C.-L., Yin X.-F., Ge R., Zhang L.-H., He Q.-Y. Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumoniae. Journal of Proteome Research 2010, 9:275-282.
21. Reinders J., Wagner K., Zahedi R.P., Stojanovski D., Eyrich B., van der Laan M., Rehling P., Sickmann A., Pfanner N., Meisinger C. Profiling phosphoproteins of yeast mitochondria reveals a role of phosphorylation in assembly of the ATP synthase. Molecular & Cellular Proteomics: MCP 2007, 6:1896-1906.
22. Fiedler D., Braberg H., Mehta M., Chechik G., Cagney G., Mukherjee P., Silva A.C., Shales M., Collins S.R., van Wageningen S., et al. Functional organization of the S. cerevisiae phosphorylation network. Cell 2009, 136:952-963.
23. van Wageningen S., Kemmeren P., Lijnzaad P., Margaritis T., Benschop J.J., de Castro I.J., van Leenen D., Groot Koerkamp M.J.A., Ko C.W., Miles A.J. Functional overlap and regulatory links shape genetic interactions between signaling pathways. Cell 2010, 143:991-1004.
24. Breitkreutz A., Choi H., Sharom J.R., Boucher L., Neduva V., Larsen B., Lin Z.Y., Breitkreutz B.J., Stark C., Liu G., et al. A global protein kinase and phosphatase interaction network in yeast. Science 2010, 328:1043-1046.
25. Yachie N., Saito R., Sugiyama N., Tomita M., Ishihama Y. Integrative features of the yeast phosphoproteome and protein-protein interaction map. PLoS Computational Biology 2011, 7:e1001064.
26. Zhang Z., Tan M., Xie Z., Dai L., Chen Y., Zhao Y. Identification of lysine succinylation as a new post-translational modification. Nature Chemical Biology 2010, 7:58-63.
27. Zhao S., Xu W., Jiang W., Yu W., Lin Y., Zhang T., Yao J., Zhou L., Zeng Y., Li H., et al. Regulation of cellular metabolism by protein lysine acetylation. Science (New York, NY) 2010, 327:1000-1004.
28. Wang Q., Zhang Y., Yang C., Xiong H., Lin Y., Yao J., Li H., Xie L., Zhao W., Yao Y., et al. Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science (New York, NY) 2010, 327:1004-1007.
29. Pearce M.J., Mintseris J., Ferreyra J., Gygi S.P., Darwin K.H. Ubiquitin-like protein involved in the proteasome pathway of Mycobacterium tuberculosis. Science (New York, NY) 2008, 322:1104-1107.
30. Poulsen C., Akhter Y., Jeon A.H.-W., Schmitt-Ulms G., Meyer H.E., Stefanski A., Stühler K., Wilmanns M., Song Y.-H. Proteome-wide identification of mycobacterial pupylation targets. Molecular Systems Biology 2010, 6:386.
31. Hardiman T., Meinhold H., Hofmann J., Ewald J.C., Siemann-Herzberg M., Reuss M. Prediction of kinetic parameters from DNA-binding site sequences for modeling global transcription dynamics in Escherichia coli. Metabolic Engineering 2010, 12:196-211.
32. Savageau M.A. Biomedical engineering strategies in system design space. Annals of Biomedical Engineering 2011, 39:1278-1295.
33. Gallego O., Betts M.J., Gvozdenovic-Jeremic J., Maeda K., Matetzki C., Aguilar-Gurrieri C., Beltran-Alvarez P., Bonn S., Fernández-Tornero C., Jensen L.J., et al. A systematic screen for protein-lipid interactions in Saccharomyces cerevisiae. Molecular Systems Biology 2010, 6.
34. Tagore R., Thomas H.R., Homan E.A., Munawar A., Saghatelian A. A global metabolite profiling approach to identify protein-metabolite interactions. Journal of the American Chemical Society 2008, 130:14111-14113.
35. Li X., Gianoulis T.A., Yip K.Y., Gerstein M., Snyder M. Extensive in vivo metabolite-protein interactions revealed by large-scale systematic analyses. Cell 2010, 143:639-650.
36. Bradley P.H., Brauer M.J., Rabinowitz J.D., Troyanskaya O.G. Coordinated concentration changes of transcripts and metabolites in Saccharomyces cerevisiae. PLoS Computational Biology 2009, 5:e1000270.
37. Narayanaswamy R., Levy M., Tsechansky M., Stovall G.M., O'Connell J.D., Mirrielees J., Ellington A.D., Marcotte E.M. Widespread reorganization of metabolic enzymes into reversible assemblies upon nutrient starvation. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:10147-10152.
38. Tanaka S., Sawaya M.R., Yeates T.O. Structure and mechanisms of a protein-based organelle in Escherichia coli. Science (New York, NY) 2010, 327:81-84.
39. Meyer F.M., Gerwig J., Hammer E., Herzberg C., Commichau F.M., Völker U., Stülke J. Physical interactions between tricarboxylic acid cycle enzymes in Bacillus subtilis: evidence for a metabolon. Metabolic Engineering 2010, 13:18-27.
40. Savage D.F., Afonso B., Chen A.H., Silver P.A. Spatially ordered dynamics of the bacterial carbon fixation machinery. Science (New York, NY) 2010, 327:1258-1261.
41. Møller B.L. Plant science. Dynamic metabolons. Science (New York, NY) 2010, 330:1328-1329.
42. Gianchandani E.P., Joyce A.R., Palsson B., Papin J.A. Functional states of the genome-scale Escherichia coli transcriptional regulatory system. PLoS Computational Biology 2009, 5:e1000403.
43. Barua D., Kim J., Reed J.L. An automated phenotype-driven approach (GeneForce) for refining metabolic and regulatory models. PLoS Computational Biology 2010, 6:e1000970.
44. Shlomi T., Eisenberg Y., Sharan R., Ruppin E. A genome-scale computational study of the interplay between transcriptional regulation and metabolism. Molecular Systems Biology 2007, 3:101.
45. Krishna S., Orosz L., Sneppen K., Adhya S., Semsey S. Relation of intracellular signal levels and promoter activities in the gal regulon of Escherichia coli. Journal of Molecular Biology 2009, 391:671-678.
46. Davidson C.J., Narang A., Surette M.G. Integration of transcriptional inputs at promoters of the arabinose catabolic pathway. BMC Systems Biology 2010, 4:75.
47. Kaplan S., Bren A., Zaslaver A., Dekel E., Alon U. Diverse two-dimensional input functions control bacterial sugar genes. Molecular Cell 2008, 29:786-792.
48. Brynildsen M.P., Liao J.C. An integrated network approach identifies the isobutanol response network of Escherichia coli. Molecular Systems Biology 2009, 5:277.
49. Chechik G., Oh E., Rando O., Weissman J., Regev A., Koller D. Activity motifs reveal principles of timing in transcriptional control of the yeast metabolic network. Nature Biotechnology 2008, 26:1251-1259.
50. Ralser M., Wamelink M.M.C., Latkolik S., Jansen E.E.W., Lehrach H., Jakobs C. Metabolic reconfiguration precedes transcriptional regulation in the antioxidant response. Nature Biotechnology 2009, 27:604-605.
51. Bennett M.R., Pang W.L., Ostroff N.A., Baumgartner B.L., Nayak S., Tsimring L.S., Hasty J. Metabolic gene regulation in a dynamically changing environment. Nature 2008, 454:1119-1122.
52. Kim H.D., Shay T., O'Shea E.K., Regev A. Transcriptional regulatory circuits: predicting numbers from alphabets. Science (New York, NY) 2009, 325:429-432.
53. Hyduke D.R., Palsson B. Towards genome-scale signalling-network reconstructions. Nature Reviews. Genetics 2010, 11:297-307.
54. Zi Z., Liebermeister W., Klipp E. A quantitative study of the Hog1 MAPK response to fluctuating osmotic stress in Saccharomyces cerevisiae. PLoS ONE 2010, 5:e9522.
55. Kuttykrishnan S., Sabina J., Langton L.L., Johnston M., Brent M.R. A quantitative model of glucose signaling in yeast reveals an incoherent feed forward loop leading to a specific, transient pulse of transcription. Proceedings of the National Academy of Sciences 2010, 107:16743-16748.
56. Usaite R., Jewett M.C., Oliveira A.P., Yates J.R., Olsson L., Nielsen J. Reconstruction of the yeast Snf1 kinase regulatory network reveals its role as a global energy regulator. Molecular Systems Biology 2009, 5:319.
57. Grüning N.-M., Lehrach H., Ralser M. Regulatory crosstalk of the metabolic network. Trends in Biochemical Sciences 2010, 35:220-227.
58. Zhang J., Lau M.W., Ferré-D'Amaré A.R. Ribozymes and riboswitches: modulation of RNA function by small molecules. Biochemistry 2010, 49:9123-9131.
59. Kotte O., Zaugg J.B., Heinemann M. Bacterial adaptation through distributed sensing of metabolic fluxes. Molecular Systems Biology 2010, 6:355.
60. Christen S., Sauer U. Intracellular characterization of aerobic glucose metabolism in seven yeast species by (13) C flux analysis and metabolomics. FEMS Yeast Research 2011, 11:263-272.
61. Kremling A., Bettenbrock K., Gilles E.D. A feed-forward loop guarantees robust behavior in Escherichia coli carbohydrate uptake. Bioinformatics (Oxford, England) 2008, 24:704-710.
62. Goelzer A., Bekkal Brikci F., Martin-Verstraete I., Noirot P., Bessières P., Aymerich S., Fromion V. Reconstruction and analysis of the genetic and metabolic regulatory networks of the central metabolism of Bacillus subtilis. BMC Systems Biology 2008, 2:20.
63. Yuan J., Doucette C.D., Fowler W.U., Feng X.-J., Piazza M., Rabitz H.A., Wingreen N.S., Rabinowitz J.D. Metabolomics-driven quantitative analysis of ammonia assimilation in E. coli. Molecular Systems Biology 2009, 5:302.
64. Bennett B.D., Kimball E.H., Gao M., Osterhout R., Van Dien S.J., Rabinowitz J.D. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nature Chemical Biology 2009, 5:593-599.
65. Fendt S.-M., Buescher J.M., Rudroff F., Picotti P., Zamboni N., Sauer U. Tradeoff between enzyme and metabolite efficiency maintains metabolic homeostasis upon perturbations in enzyme capacity. Molecular Systems Biology 2010, 6:356.
66. Westerhoff H.V., Kolodkin A., Conradie R., Wilkinson S.J., Bruggeman F.J., Krab K., van Schuppen J.H., Hardin H., Bakker B.M., Moné M.J., et al. Systems biology towards life in silico: mathematics of the control of living cells. Journal of Mathematical Biology 2009, 58:7-34.
67. Fendt S.-M., Oliveira A.P., Christen S., Picotti P., Dechant R.C., Sauer U. Unraveling condition-dependent networks of transcription factors that control metabolic pathway activity in yeast. Molecular Systems Biology 2010, 6:432.
68. Haverkorn van Rijsewijk B.R.B., Nanchen A., Nallet S., Kleijn R.J., Sauer U. Large-scale 13C-flux analysis reveals distinct transcriptional control of respiratory and fermentative metabolism in Escherichia coli. Molecular Systems Biology 2011, 7:477.
69. Kleijn R.J., Buescher J.M., Le Chat L., Jules M., Aymerich S., Sauer U. Metabolic fluxes during strong carbon catabolite repression by malate in Bacillus subtilis. The Journal of Biological Chemistry 2010, 285:1587-1596.
70. Bordel S., Agren R., Nielsen J. Sampling the solution space in genome-scale metabolic networks reveals transcriptional regulation in key enzymes. PLoS Computational Biology 2010, 6:e1000859.
71. Costenoble R., Picotti P., Reiter L., Stallmach R., Heinemann M., Sauer U., Aebersold R. Comprehensive quantitative analysis of central carbon and amino-acid metabolism in Saccharomyces cerevisiae under multiple conditions by targeted proteomics. Molecular Systems Biology 2011, 7:464.
72. Maier K., Hofmann U., Reuss M., Mauch K. Dynamics and control of the central carbon metabolism in hepatoma cells. BMC Systems Biology 2010, 4:54.
73. Rossell S., Solem C., Jensen P.R., Heijnen J.J. Towards a quantitative prediction of the fluxome from the proteome. Metabolic Engineering 2011, 13:253-262.
74. Daran-Lapujade P., Rossell S., van Gulik W.M., Luttik M.A.H., de Groot M.J.L., Slijper M., Heck A.J.R., Daran J.-M., de Winde J.H., Westerhoff H.V., et al. The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:15753-15758.
75. van Eunen K., Bouwman J., Lindenbergh A., Westerhoff H.V., Bakker B.M. Time-dependent regulation analysis dissects shifts between metabolic and gene-expression regulation during nitrogen starvation in baker's yeast. The FEBS Journal 2009, 276:5521-5536.
76. Curien G., Bastien O., Robert-Genthon M., Cornish-Bowden A., Cárdenas M.L., Dumas R. Understanding the regulation of aspartate metabolism using a model based on measured kinetic parameters. Molecular Systems Biology 2009, 5:271.
77. Wright K.M., Rausher M.D. The evolution of control and distribution of adaptive mutations in a metabolic pathway. Genetics 2010, 184:483-502.
78. Molenaar D., Berlo R., van Ridder D., de Teusink B. Shifts in growth strategies reflect tradeoffs in cellular economics. Molecular Systems Biology 2009, 5:323.
79. Lewis N.E., Hixson K.K., Conrad T.M., Lerman J.A., Charusanti P., Polpitiya A.D., Adkins J.N., Schramm G., Purvine S.O., Lopez-Ferrer D., et al. Omic data from evolved E. coli are consistent with computed optimal growth from genome-scale models. Molecular Systems Biology 2010, 6.
80. Dekel E., Alon U. Optimality and evolutionary tuning of the expression level of a protein. Nature 2005, 436:588-592.
81. Shou C., Bhardwaj N., Lam H.Y.K., Yan K.-K., Kim P.M., Snyder M., Gerstein M.B. Measuring the evolutionary rewiring of biological networks. PLoS Computational Biology 2011, 7:e1001050.
82. Isalan M., Lemerle C., Michalodimitrakis K., Horn C., Beltrao P., Raineri E., Garriga-Canut M., Serrano L. Evolvability and hierarchy in rewired bacterial gene networks. Nature 2008, 452:840-845.
83. Shinar G., Rabinowitz J.D., Alon U. Robustness in glyoxylate bypass regulation. PLoS Computational Biology 2009, 5:e1000297.
84. Chin C.-S., Chubukov V., Jolly E.R., DeRisi J., Li H. Dynamics and design principles of a basic regulatory architecture controlling metabolic pathways. PLoS Biology 2008, 6:e146.
85. Savageau M.A., Coelho P.M.B.M., Fasani R.A., Tolla D.A., Salvador A. Phenotypes and tolerances in the design space of biochemical systems. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:6435-6440.
86. Tolla D.A., Savageau M.A. Phenotypic repertoire of the FNR regulatory network in Escherichia coli. Molecular Microbiology 2010, 79:149-165.
87. Buchakjian M.R., Kornbluth S The engine driving the ship: metabolic steering of cell proliferation and death. Nature Reviews. Molecular Cell Biology 2010, 11:715-727.