Super life - How and why 'cell selection' leads to the fastest-growing eukaryote

FEBS Journal

Volumn 276, Issue 1, 2009, Pages 254-270

  Groeneveld, Philip ^a   Stouthamer, Adriaan H ^a   Westerhoff, Hans V ^a,b,c  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Highest eukaryotic growth rate; Modular control analysis; pH auxostat selection; Surface to volume ratio optimization; Systems biology

Indexed keywords

ANIMAL CELL; ARTICLE; CELL CYCLE; CELL GROWTH; CELL SELECTION; CELL SURFACE; CELL VOLUME; EUKARYOTE; KLUYVEROMYCES; KLUYVEROMYCES MARXIANUS; NONHUMAN; PRIORITY JOURNAL;

CELL CYCLE; CULTURE MEDIA; EUKARYOTIC CELLS; GROWTH; HYDROGEN-ION CONCENTRATION; KINETICS; KLUYVEROMYCES; REPRODUCTION; SELECTION (GENETICS); SPECIES SPECIFICITY;

EUKARYOTA; KLUYVEROMYCES MARXIANUS;

EID: 57649219146     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06778.x     Document Type: Article

References (92)

1. Groeneveld P (1999) Control of specific growth rate and physiology of the yeast Kluyveromyces marxianus; a biothermokinetic approach. Thesis, pp. 1 324 (ISBN 90-9013010-1 Departments of Molecular Cell Physiology & Mathematical Biochemistry, Vrije Universiteit Amsterdam, The Netherlands.
2. Aiyar SE, Gaal T Gourse RL (2002) rRNA promoter activity in the fast-growing bacterium Vibrio natriegens. J Bacteriol 184, 1349 1358.
3. Eagon RG (1962) Pseudomonas natriegens, a marine bacterium with a generation time of less than 10 minutes. J Bacteriol 83, 736 737.
4. Bergkamp RJM, Bootsman TC, Toschka HY, Mooren ATA, Kox L, Verbakel JMA, Geerse RH Planta RJ (1993) Expression of an B-galactosidase gene under control of the homologous inulinase promoter in Kluyveromyces marxianus. Appl Microbiol Biotechnol 40, 309 317.
5. Chapman JW, Musters W, Rouwenhorst RJ, Toschka HY Verbakel JMA (1994). The use of the Kluyveromyces marxianus inulinase gene promoter for protein production. World wide patent WO 9413821.
6. Hensing M, Vrouwenvelder H, Hellinga C, Baartmans R Dijken H (1994) Production of extracellular inulinase in high-cell-density fed-batch cultures of Kluyveromyces marxianus. Appl Microbiol Biotechnol 42, 516 521.
7. Hensing MCM, Rouwenhorst RJ, Heijnen JJ, Dijken JP Pronk JT (1995) Physiological and technological aspects of large-scale heterologous-protein production with yeasts. Antonie Van Leeuwenhoek 67, 261 279.
8. Koster JG, Destree OH Westerhoff HV (1988) Kinetics of histone gene expression during early development of Xenopus laevis. J Theor Biol 135, 139 167.
9. Groeneveld P, Van Verseveld HW, Van Dam K Stouthamer AH (1990) Optimization of the maximal growth rate of industrial yeasts: optimization with the use of MCA and MNET. In Biothermokinetics (Westerhoff HV, ed pp. 397 403. Intercept Ltd, Andover.
10. Westerhoff HV Van Dam K (1987) Thermodynamics and Control of Biological Free-Energy Transduction. Elsevier, Amsterdam.
11. Groeneveld P, Jeronimus E, Van Dam K, Stouthamer AH Van Verseveld HW (1992) Optimization of the maximal growth rate of industrial yeasts: optimization with the use of the metabolic control theory and mosaic non-equilibrium thermodynamics. In Modern Trends in Biothermokinetics (Schuster S, Rigoulet M, Ouhabi R Mazat J-P, eds pp. 397 403. Plenum Press, London.
12. Fell DA (1992) Metabolic control analysis: a survey of its theoretical and experimental development. Biochem J 286, 313 330.
13. Heinrich R Rapoport TA (1974) A linear steady-state treatment of enzymatic chains. General properties, control and effector strength. Eur J Biochem 42, 89 95.
14. Kacser H Burns JA (1973) The control of flux. Symp Soc Exp Biol 27, 65 104.
15. van der Aar PC, van den Heuvel JJ, Roling WF, Raue HA, Stouthamer AH van Verseveld HW (1992) Effects of phosphoglycerate kinase overproduction in Saccharomyces cerevisiae on the physiology and plasmid stability. Yeast 8, 47 55.
16. Reijenga KA, Snoep JL, Diderich JA, van Verseveld HW, Westerhoff HV Teusink B (2001) Control of glycolytic dynamics by hexose transport in Saccharomyces cerevisiae. Biophys J 80, 626 634.
17. Schaaff I, Heinisch J Zimmermann FK (1989) Overproduction of glycolytic enzymes in yeast. Yeast 5, 285 290.
18. van Dam K, Jansen N, Postma P, Richard P, Ruijter G, Rutgers M, Smits HP, Teusink B, van der Vlag J, Walsh M et al. (1993) Control and regulation of metabolic fluxes in microbes by substrates and enzymes. Antonie Van Leeuwenhoek 63, 315 321.
19. Ye L, Kruckeberg AL, Berden JA van Dam K (1999) Growth and glucose repression are controlled by glucose transport in Saccharomyces cerevisiae cells containing only one glucose transporter. J Bacteriol 181, 4673 4675.
20. Teusink B, Diderich JA, Westerhoff HV, van Dam K Walsh MC (1998) Intracellular glucose concentration in derepressed yeast cells consuming glucose is high enough to reduce the glucose transport rate by 50%. J Bacteriol 180, 556 562.
21. Teusink B, Passarge J, Reijenga CA, Esgalhado E, van der Weijden CC, Schepper M, Walsh MC, Bakker BM, van Dam K, Westerhoff HV et al. (2000) Can yeast glycolysis be understood in terms of in vitro kinetics of the constituent enzymes? Testing biochemistry. Eur J Biochem 267, 5313 5329.
22. van der Vlag J, van't Hof R, van Dam K Postma PW (1995) Control of glucose metabolism by the enzymes of the glucose phosphotransferase system in Salmonella typhimurium. Eur J Biochem 230, 170 182.
23. Dykhuizen DE, Dean AM Hartl DL (1987) Metabolic flux and fitness. Genetics 115, 25 31.
24. Jensen PR, Michelsen O Westerhoff HV (1993) Control analysis of the dependence of Escherichia coli physiology on the H(+)-ATPase. Proc Natl Acad Sci USA 90, 8068 8072.
25. Fell DA (1998) Increasing the flux in metabolic pathways: a metabolic control analysis perspective. Biotechnol Bioeng 58, 121 124.
26. Bakker BM, Michels PA, Opperdoes FR Westerhoff HV (1999) What controls glycolysis in bloodstream form Trypanosoma brucei? J Biol Chem 274, 14551 14559.
27. Flint HJ, Tateson RW, Barthelmess IB, Porteous DJ, Donachie WD Kacser H (1981) Control of the flux in the arginine pathway of Neurospora crassa. Modulations of enzyme activity and concentration. Biochem J 200, 231 246.
28. Groen AK, Wanders RJ, Westerhoff HV, van der Meer R Tager JM (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257, 2754 2757.
29. Thomas S, Mooney PJ, Burrell MM Fell DA (1997) Finite change analysis of glycolytic intermediates in tuber tissue of lines of transgenic potato (Solanum tuberosum) overexpressing phosphofructokinase. Biochem J 322, 111 117.
30. Torres NV, Mateo F, Melendez-Hevia E Kacser H (1986) Kinetics of metabolic pathways. A system in vitro to study the control of flux. Biochem J 234, 169 174.
31. Haanstra JR, Stewart M, Luu VD, Tuijl AV, Westerhoff HV, Clayton C Bakker BM (2007) Control and regulation of gene expression: quantitative analysis of the expression of phosphoglycerate kinase in bloodstream form Trypanosoma brucei. J Biol Chem 283, 2495 2507.
32. Kacser H Acerenza L (1993) A universal method for achieving increases in metabolite production. Eur J Biochem 216, 361 367.
33. Kholodenko BN, Westerhoff HV, Schwaber J Cascante M (2000) Engineering a living cell to desired metabolite concentrations and fluxes: pathways with multifunctional enzymes. Metab Eng 2, 1 13.
34. Kholodenko BN, Schuster S, Rohwer JM, Cascante M Westerhoff HV (1995) Composite control of cell function: metabolic pathways behaving as single control units. FEBS Lett 368, 1 4.
35. Raamsdonk LM, Teusink B, Broadhurst D, Zhang N, Hayes A, Walsh MC, Berden JA, Brindle KM, Kell DB, Rowland JJ et al. (2001) A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat Biotechnol 19, 45 50.
36. Hofmeyr JH Westerhoff HV (2001) Building the cellular puzzle: control in multi-level reaction networks. J Theor Biol 208, 261 285.
37. Reitzer LJ (1996) Cellular and Molecular Biology. American Society for Microbiology, Washington DC.
38. Hoekstra R, Groeneveld P, Van Verseveld HW, Stouthamer AH Planta RJ (1994) Transcription regulation of ribosomal protein genes at different growth rates in continuous cultures of Kluyveromyces yeasts. Yeast 10, 637 651.
39. Brown AJ, Planta RJ, Restuhadi F, Bailey DA, Butler PR, Cadahia JL, Cerdan ME, De Jonge M, Gardner DC, Gent ME et al. (2001) Transcript analysis of 1003 novel yeast genes using high-throughput Northern hybridizations. EMBO J 20, 3177 3186.
40. Herruer MH, Mager WH, Woudt LP, Nieuwint RT, Wassenaar GM, Groeneveld P Planta RJ (1987) Transcriptional control of yeast ribosomal protein synthesis during carbon-source upshift. Nucleic Acids Res 15, 10133 10144.
41. Westerhoff HV (2001) The silicon cell, not dead but live! Metab Eng 3, 207 210.
42. Clegg JS, Jackson SA Fendl K (1990) Effects of reduced cell volume and water content on glycolysis in L-929 cells. J Cell Physiol 142, 386 391.
43. Koch AL (1996) What size should a bacterium be? A question of scale. Annu Rev Microbiol 50, 317 348.
44. Kooijman SALM (1993) Dynamic Energy Budgets in Biological Systems. Cambridge University Press, Cambridge.
45. Kooijman SALM (2000) Dynamic Energy and Mass Budgets in Biological Systems. Cambridge University Press, Cambridge.
46. Hennaut C, Hilger F Grenson M (1970) Space limitation for permease insertion in the cytoplasmic membrane of Saccharomyces cerevisiae. Biochem Biophys Res Commun 39, 666 671.
47. Grenson M (1969) The utilization of exogenous pyrimidines and the recycling of uridine-5′-phosphate derivatives in Saccharomyces cerevisiae, as studied by means of mutants affected in pyrimidine uptake and metabolism. Eur J Biochem 11, 249 260.
48. Grenson M, Mousset M, Wiame JM Bechet J (1966) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. I. Evidence for a specific arginine-transporting system. Biochim Biophys Acta 127, 325 338.
49. Grenson M (1966) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. II. Evidence for a specific lysine-transporting system. Biochim Biophys Acta 127, 339 346.
50. Gits JJ Grenson M (1967) Multiplicity of the amino acid permeases in Saccharomyces cerevisiae. III. Evidence for a specific methionine-transporting system. Biochim Biophys Acta 135, 507 516.
51. Ferea TL, Botstein D, Brown PO Rosenzweig RF (1999) Systematic changes in gene expression patterns following adaptive evolution in yeast. Proc Natl Acad Sci USA 96, 9721 9726.
52. Baganz F, Hayes A, Farquhar R, Butler PR, Gardner DC Oliver SG (1998) Quantitative analysis of yeast gene function using competition experiments in continuous culture. Yeast 14, 1417 1427.
53. Snoep JL, Jensen PR, Groeneveld P, Molenaar D, Kholodenko BN Westerhoff HV (1994) How to determine control of growth rate in a chemostat. Using metabolic control analysis to resolve the paradox. Biochem Mol Biol Int 33, 1023 1032.
54. Davey HM, Davey CL, Woodward AM, Edmonds AN, Lee AW Kell DB (1996) Oscillatory, stochastic and chaotic growth rate fluctuations in permittistat-controlled yeast cultures. Biosystems 39, 43 61.
55. Groeneveld P, Stouthamer AH Van Verseveld HW (1994) Energy metabolism and growth kinetics of Kluyveromyces marxianus in oxygen-dependent pH-auxostat culture. In What Is Controlling Life? (Gnaiger E, Gellerich FN Wyss M, eds pp. 254 256. Innsbruck University Press, Innsbruck, Austria.
56. Martin GA Hempfling WP (1976) A method for the regulation of microbial population density during continuous culture at high growth rates. Arch Microbiol 107, 41 47.
57. Snoep JL, Rohwer JM Hofmeyr JH (2006) 12th BTK meeting: 'systems biology: redefining biothermokinetics'. Syst Biol 153, 312 313.
58. Bruggeman FJ, Westerhoff HV Boogerd FC (2002) BioComplexity: a pluralist research strategy is necessary for a mechanistic explanation of the 'live' state. Philosophical Psychology 15, 411 440.
59. Westerhoff HV, Jensen PR, Snoep JL Kholodenko BN (1998) Thermodynamics of complexity. The live cell. Thermochim Acta 309, 111 120.
60. Hutchison CA, Peterson SN, Gill SR, Cline RT, White O, Fraser CM, Smith HO Venter JC (1999) Global transposon mutagenesis and a minimal Mycoplasma genome. Science 286, 2165 2169.
61. Lasa I Berenguer J (1993) Thermophilic enzymes and their biotechnological potential. Microbiologia 9, 77 89.
62. van Urk H, Postma E, Scheffers WA van Dijken JP (1989) Glucose transport in Crabtree-positive and Crabtree-negative yeasts. J Gen Microbiol 135, 2399 2406.
63. Lopes TS, Klootwijk J, Veenstra AE, van der Aar PC, van Heerikhuizen H, Raue HA Planta RJ (1989) High-copy-number integration into the ribosomal DNA of Saccharomyces cerevisiae: a new vector for high-level expression. Gene 79, 199 206.
64. Snoep JL, Bruggeman F, Olivier BG Westerhoff HV (2005) Towards building the silicon cell: a modular approach. Biosystems 83, 207 216.
65. Lodder J Kreger-van Rij NJW (1970) A Taxonomic Study in the Yeasts. North-Holland Publishing Company, New York, NY.
66. Schuster S, Kahn D Westerhoff HV (1993) Modular analysis of the control of complex metabolic pathways. Biophys Chem 48, 1 17.
67. Schuster S (1999) Use and limitations of modular metabolic control analysis in medicine and biotechnology. Metab Eng 1, 232 242.
68. ter Kuile B Westerhoff H (2001) Transcriptome meets metabolome: hierarchical and metabolic regulation of the glycolytic pathway. FEBS Lett 500, 169 171.
69. Stemmer WP (1994) Rapid evolution of a protein in vitro by DNA shuffling. Nature 370, 389 391.
70. Koebmann BJ, Westerhoff HV, Snoep JL, Nilsson D Jensen PR (2002) The glycolytic flux in Escherichia coli is controlled by the demand for ATP. J Bacteriol 184, 3909 3916.
71. Mongold JA Lenski RE (1996) Experimental rejection of a nonadaptive explanation for increased cell size in Escherichia coli. J Bacteriol 178, 5333 5334.
72. Wheals AE Lord PG (1992) Clonal heterogeneity in specific growth rate of Saccharomyces cerevisiae cells. Cell Prolif 25, 217 223.
73. Axelrod DE, Gusev Y Kuczek T (1993) Persistence of cell cycle times over many generations as determined by heritability of colony sizes of ras oncogene-transformed and non-transformed cells. Cell Prolif 26, 235 249.
74. Kimmel M, Darzynkiewicz Z, Arino O Traganos F (1984) Analysis of a cell cycle model based on unequal division of metabolic constituents to daughter cells during cytokinesis. J Theor Biol 110, 637 664.
75. Lolle SJ, Victor JL, Young JM Pruitt RE (2005) Genome-wide non-Mendelian inheritance of extra-genomic information in Arabidopsis. Nature 434, 505 509.
76. Chaudhury A (2005) Plant genetics: hothead healer and extragenomic information. Nature 437, doi :.
77. Weigel D Jurgens G (2005) Genetics: hotheaded healer. Nature 434, 443.
78. Ray A (2005) Plant genetics: RNA cache or genome trash? Nature 437, doi :.
79. Kocková-Kratochvílová A (1990) Yeasts and Yeast-Like Organisms. VCH Publishers, New York, NY.
80. Dean AM, Dykhuizen DE Hartl DL (1986) Fitness as a function of beta-galactosidase activity in Escherichia coli. Genet Res 48, 1 8.
81. Kholodenko BN, Rohwer JM, Cascante M Westerhoff HV (1998) Subtleties in control by metabolic channelling and enzyme organization. Mol Cell Biochem 184, 311 320.
82. Cooper S (1991) Bacterial Growth and Division: Biochemistry and Regulation of Prokaryotic and Eukaryotic Division Cycles. Academic Press, New York, NY.
83. Cooper S (2006) Regulation of DNA synthesis in bacteria: analysis of the Bates/Kleckner licensing/initiation-mass model for cell cycle control. Mol Microbiol 62, 303 307.
84. Planta RJ Raue HA (1988) Control of ribosome biogenesis in yeast. Trends Genet 4, 64 68.
85. Rashevsky N (1961) Mathematical biology. Conn Med 25, 176 177.
86. Groeneveld P, Rolley N, Kell DB, Kelly SL Kelly DE (2002) Metabolic control analysis and engineering of the yeast sterol biosynthetic pathway. Mol Biol Rep 29, 27 29.
87. Powell CD, Quain DE Smart KA (2003) Chitin scar breaks in aged Saccharomyces cerevisiae. Microbiology 149, 3129 3137.
88. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, Christmas R, Avila-Campilo I, Creech M, Gross B et al. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat Protoc 2, 2366 2382.
89. Duarte NC, Herrgard MJ Palsson BO (2004) Reconstruction and validation of Saccharomyces cerevisiae iND750, a fully compartmentalized genome-scale metabolic model. Genome Res 14, 1298 1309.
90. Joyce AR Palsson BO (2006) The model organism as a system: integrating 'omics' data sets. Nat Rev Mol Cell Biol 7, 198 210.
91. Nelissen B, De Wachter R Goffeau A (1997) Classification of all putative permeases and other membrane plurispanners of the major facilitator superfamily encoded by the complete genome of Saccharomyces cerevisiae. FEMS Microbiol Rev 21, 113 134.
92. Herbert D, Phipps PJ Strange RE (1971) Chemical analysis of microbial cells. In Methods in Microbiology, Vol. 5B (Norris JR Ribbons DW, eds pp. 209 344. Academic Press, New York, NY.