Five-step continuous production of PHB analyzed by elementary flux, modes, yield space analysis and high structured metabolic model

Biochemical Engineering Journal

Volumn 79, Issue , 2013, Pages 57-70

  Lopar, Markan ^a   Vrana Špoljarić, Ivna ^a   Atlić, Aid ^b   Koller, Martin ^b   Braunegg, Gerhart ^b   Horvat, Predrag ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

Author keywords

Cupriavidus necator; Elementary modes; High structured mathematical model; Metabolic fluxes; Poly(3 Hydroxybutyrate); Yield space analysis

Indexed keywords

CUPRIAVIDUS NECATOR; ELEMENTARY MODE; METABOLIC FLUX; POLY-3-HYDROXYBUTYRATE; SPACE ANALYSIS;

MATHEMATICAL MODELS;

METABOLISM;

GLUCOSE; GLUCOSE 6 PHOSPHATE ISOMERASE; POLY(3 HYDROXYBUTYRIC ACID);

AERATION; ARTICLE; BIOMASS; BIOREACTOR; CELL METABOLISM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CUPRIAVIDUS NECATOR; DILUTION; ENZYME ACTIVITY; FLOW RATE; INTRACELLULAR SPACE; MATHEMATICAL MODEL; NONHUMAN; PRIORITY JOURNAL; SPACE; SYNTHESIS;

EID: 84881116361     PISSN: 1369703X     EISSN: 1873295X     Source Type: Journal    
DOI: 10.1016/j.bej.2013.07.003     Document Type: Article

References (76)

1. Biopolymers, vol. 3b: Polyesters 2001, 480. Wiley-VCH, Weinheim. Y. Doi, A. Steinbüchel (Eds.).
2. Koller M., Salerno A., Dias M., Reiterer A., Braunegg G. Modern biotechnological polymer synthesis-a review. Food Technol. Biotechnol. 2010, 48:255-269.
3. Steinbüchel A., Schlegel H.G. Physiology and molecular genetics of poly(b-hydroxyalkanoic acid) synthesis in Alcaligenes eutrophus. Mol. Microbiol. 1991, 5:535-542.
4. Koller M., Gasser I., Schmid F., Berg G. Linking ecology with economy: insights into polyhydroxyalkanoate-producing microorganisms. Eng. Life Sci. 2011, 11:222-237.
5. Steinbüchel A., Füchtenbusch B. Bacterial and other biological systems for polyester production. Trends Biotechnol. 1998, 16:419-427.
6. Braunegg G., Koller M., Varila P., Kutschera C., Bona R., Hermann C., Horvat P., Neto J., Pereira L. Production of plastics from waste derived from agrofood industry. Renewable Resources and Renewable Energy 2007, 119-135. University of Trieste, Trieste. P. Fornasiero, M. Graziani (Eds.).
7. Lee S.Y. Plastic bacteria? Progress and prospects for polyhydroxyalkanoate production in bacteria. Trends Biotechnol. 1996, 14:431-438.
8. Lee S.Y. Bacterial polyhydroxyalkanoates. Biotechnol. Bioeng. 1996, 49:1-14.
9. Chen G.Q. A microbial polyhydroxyalkanoates (PHA) based bio- and materials industry. Chem. Soc. Rev. 2009, 38:2434-2446.
10. Khanna S., Srivastava A. Recent advances in microbial polyhydroxyalkanoates. Process Biochem. 2005, 40:607-619.
11. Reddy C.S.K., Ghai R., Rashmi K.V.C. Polyhydroxyalkanoates: an overview. Bioresour. Technol. 2003, 87:137-146.
12. Ren Q., Grubelnik A., Hoerler M., Ruth K., Hartmann R., Felber H., Zinn M. Bacterial poly(hydroxyalkanoates) as a source of chiral hydroxyalkanoic acids. Biomacromolecules 2005, 6:2290-2298.
13. Choi J., Lee S.Y. Factors affecting the economics of polyhydroxyalkanoate production by bacterial fermentation. Appl. Microbiol. Biotechnol. 1999, 51:13-21.
14. Koller M., Hesse P., Kutschera C., Bona R., Nascimento J., Ortega S., Agnelli J., Braunegg G. Sustainable embedding of the bioplastic poly-(3-hydroxybutyrate) into sugarcane industry: principles of a future-oriented technology in Brazil. Polymers-Opportunities and Risks 2010, vol. II:81-96. Springer-Verlag, Berlin Heidelberg.
15. Sudesh K., Iwata T. Sustainability of biobased and biodegradable plastics. Clean Soil Air Water 2008, 36:433-442. 10.1002/clen.200700183.
16. Ramsay B.A., Lomaliza K., Chavarie C., Dubé B., Bataille P., Ramsay J.A. Production of poly-(b-hydroxybutyric-co-bhydroxyvaleric) acids. Appl. Environ. Microbiol. 1990, 56:2093-2098.
17. Wilkinson J.F., Munro A.L.S. Influence of growth-limiting conditions on the synthesis of possible carbon and energy storage polymers in Bacillus megaterium. Microbial Physiology and Continuous Culture 1967, 173-185. HMSO, London. E.O. Powell, C.G.T. Evans, R.E. Strange, D.W. Tempest (Eds.).
18. Koyama N., Doi Y. Continuous production of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) by Alcaligenes eutrophus. Biotechnol. Lett. 1995, 17:281-284.
19. Yu S.T., Lin C.C., Too J.R. PHBV production by Ralstonia eutropha in a continuous stirred tank reactor. Process Biochem. 2005, 40:2729-2734.
20. Braunegg G., Genser K., Bona R., Haage G., Schellauf F., Winkler E. Production of PHAs from agricultural waste material. Macromol. Symp. 1999, 144:375-383.
21. Braunegg G., Lefebvre G., Renner G., Zeiser A., Haage G., Loidl-Lanthaler K. Kinetics as a tool for polyhydroxyalkanoate production optimization. Can. J. Microbiol. 1995, 41:239-248.
22. Hartmann R., Hany R., Pletscher E., Ritter A., Witholt B., Zinn M. Tailor-made olefinic medium-chain-length poly-[(R)-3-hydroxyalkanoates] by Pseudomonas putida GPo1: batch versus chemostat production. Biotechnol. Bioeng. 2001, 93:737-746.
23. Hartmann R., Hany R., Geiger T., Egli T., Witholt B., Zinn M. Tailored biosynthesis of olefinic medium-chain-lengthpoly[(R)-3-hydroxyalkanoates] in Pseudomonas putida GPo1with improved thermal properties. Macromolecules 2004, 37:6780-6785.
24. Ackermann J.U., Babel W. Approaches to increase the economy of the PHB production. Polym. Degrad. Stab. 1998, 59:183-186.
25. Babel W., Ackermann J.U., Breuer U. Physiology, regulation, and limits of the synthesis of poly(3HB). Advances in Biochemical Engineering/Biotechnology (Biopolyesters) 2001, vol. 71:125-157. Springer-Verlag, Berlin Heidelberg.
26. Du G., Chen J., Yu J., Lun S. Continuous production of poly-3-hydroxybutyrate by Ralstonia eutropha in a two-stage culture system. J. Biotechnol. 2001, 88:59-65.
27. Du G., Chen J., Yu J., Lun S. Kinetic studies on poly-3-hydroxybutyrate formation by Ralstonia eutropha in a two-stage continuous culture system. Process Biochem. 2001, 37:219-227.
28. Mothes G., Ackermann J.U. Synthesis of poly(3-hydroxybutyrateco-4-hydroxybutyrate) with a target mole fraction of 4-hydroxybutyric acid units by two-stage continuous cultivation of Delftia acidovorans P4a. Eng. Life Sci. 2005, 5:58-62.
29. Zinn M., Weilenmann H.U., Hany R., Schmid M., Egli T. Tailored synthesis of poly([R]-3-hydroxybutyrate-co-3-hydroxyvalerate) (PHB/HV) in Ralstonia eutropha DSM 428. Acta Biotechnol. 2003, 23:309-316.
30. Zinn M., Witholt B., Egli T. Dual nutrient limited growth: models, experimental observations, and applications. J. Biotechnol. 2004, 113:263-279.
31. Egli T. On multiple-nutrient-limited growth of microorganisms, with special reference to dual limitation by carbon and nitrogen substrates. Antonie Van Leeuwenhoek 1991, 60:225-234.
32. Egli T., Quayle J.R. Influence of the carbon: nitrogen ratio of the growth medium on the cellular composition and ability of the methylotrophic yeast Hansenula polymorpha to utilize mixed carbon sources. J. Gen. Microbiol. 1986, 132:1779-1788.
33. Wu S.T., Lin Y.C., Too J.R. Continuous production of poly(3-hydroxybutyrate-co-3-hydroxyvalerate): effects of C/N ratio and dilution rate on HB/HV ratio. Korean J. Chem. Eng. 2009, 26:411-416.
34. Atlić A., Koller M., Scherzer D., Kutschera C., Grillo-Fernandes E., Horvat P., Chiellini E., Braunegg G. Continuous production of poly([R]-3-hydroxybutyrate) by Cupriavidus necator in a multistage bioreactor cascade. Appl. Microbiol. Biotechnol. 2011, 91(2):295-304.
35. Pederson E.N., McChalicher C.W.J., Srienc F. Bacterial synthesis of PHA block copolymers. Biomacromolecules 2006, 7:1904-1911.
36. Horvat P., Vrana Špoljarić I., Lopar M., Atlić A., Koller M., Braunegg G. Mathematical modelling and process optimization of a continuous 5-stage bioreactor cascade for production of poly[-(R)-3-hydroxybutyrate] by Cupriavidus necator. Biopr. Biosyst. Eng. 2012, online ahead of press; http://dx.doi.org/10.1007/s00449-012-0852-8.
37. Stephanopoulos G.N., Aristidou A.A., Nielsen J. Metabolic Engineering: Principles and Methodologies 1998, 725. Academic Press, San Diego.
38. Gombert A.K., Nielsen J. Mathematical modeling of metabolism. Curr. Opin. Biotechnol. 2000, 11:180-186.
39. Varma A., Palsson B.Ø. Stoichiometric flux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110. Appl. Environm. Microbiol. 1994, 60:3724-3731.
40. Edwards J.S., Ramakrishna R., Schilling C.H., Palsson B.O. Metabolic flux balance analysis. Metabolic Engineering 1999, 13-57. Marcel Deker, New York. S.Y. Lee, E.T. Papoutsakis (Eds.).
41. Stelling J., Klamt S., Bettenbrock K., Schuster S., Gilles E.D. Metabolic network structure determines key aspects of functionality and regulation. Nature 2002, 420:190-1933.
42. Schuster S., Fell D.A., Dandekar T. A general definition of metabolic pathways useful for systematic organization and analysis of complex metabolic networks. Nat. Biotechnol. 2000, 18:326-332.
43. Papin J.A., Stelling J., Price N.D., Klamt S., Schuster S., Palsson B.Ø. Comparison of network-based pathway analysis methods. Trends Biotechnol. 2004, 22:400-405.
44. Papin J.A., Price N.D., Palsson B.Ø. Extreme pathway lengths and reaction participation in genome-scale metabolic networks. Genome Res. 2002, 12:1889-1900.
45. Price N.D., Papin J.A., Schilling C.H., Bernhard O., Palsson B.O. Genome-scale microbial in silico models: the constraints-based approach. Trends Biotechnol. 2003, 21:162-169.
46. Bushell M.E., Sequeira S.I.P., Khannapho C., Zhao H., Chater K.F., Butler M.J., Kierzek A.M., Avignone-Rossa C.A. The use of genome scale metabolic flux variability analysis for process feed formulation based on an investigation of the effects of the zwf mutation on antibiotic production in Streptomyces coelicolor. Enzyme Microb. Technol. 2006, 39:1347-1353.
47. Park J.M., Kim T.Y., Lee S.Y. Prediction of metabolic fluxes by incorporating genomic context and flux-converging pattern analyses. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:14931-14936.
48. Larhlimi A., Bockmayr A. A new constraint-based description of the steady-state flux cone of metabolic networks. Discrete Appl. Math. 2009, 157:2257-2266.
49. Dräger A., Kronfeld M., Ziller M.J., Supper J., Planatscher H., Magnus J.B., Oldiges M., Kohlbacher O., Zell A. Modeling metabolic networks in C. glutamicum: a comparison of rate laws in combination with various parameter optimization strategies. BMC Syst. Biol. 2009, 3:5. doi:10.1186/1752-0509-3-5.
50. Song H.S., Ramkrishna D. Reduction of a set of elementary modes using yield analysis. Biotechnol. Bioeng. 2009, 102:554-568.
51. Pohlmann A., Fricke W.F., Reinecke F., Kusian B., Liesegang H., Cramm R., Eitinger T., Ewering C., Pötter M., Schwartz E., Strittmatter A., Voss I., Gottschalk G., Steinbüchel A., Friedrich B., Bowien B. Genome sequence of the bioplastic-producing Knallgas bacterium Ralstonia eutropha H16. Nat. Biotechnol. 2006, 24:1257-1262.
52. Raberg M., Peplinski K., Heiss S., Ehrenreich A., Voigt B., Döring C., Bömeke M., Hecker M., Steinbüchel A. Proteomic and transcriptomic elucidation of the mutant Ralstonia eutropha G+1 with regard to glucose utilization. Appl. Environ. Microbiol. 2011, 77:2058-2070.
53. Franz A., Song H.S., Ramkrishna D., Kienle A., Experimental theoretical analysis of poly(β-hydroxybutyrate) formation and consumption in Ralstonia eutropha. Biochem. Eng. J. 2011, 55:49-58.
54. Park J.M., Kim T.Y., Lee S.Y. Genome-scale reconstruction and in silico analysis of the Ralstonia eutropha H16 for polyhydroxyalkanoate synthesis, litoautotrophic growth, and 2-methyl citric acid production. BMC Syst. Biol. 2011, 5:101.
55. Pfeiffer T., Sánchez-Valdenebro I., Nuño J.C., Montero F., Schuster S. METATOOL: for studying metabolic networks. Bioinformatics 1999, 15:251-257.
56. Schuster S., Dandekar T., Fell D.A. Detection of elementary flux modes in biochemical networks: a promising tool for pathway analysis and metabolic engineering. Trends Biotechnol. 1999, 17:53-60.
57. Schwartz J.M., Kanehisa M. A quadratic programming approach for decomposing steady-state metabolic flux distributions onto elementary modes. Bioinformatics 2005, 21(suppl. 2):ii204-ii205. 10.1093/bioinformatics/bti1132.
58. Poolman M.G., Venkatesh K.V., Pidcock M.K., Fell D.A. A method for the determination of flux in elementary modes, and its application to Lactobacillus rhamnosus. Biotechnol. Bioeng. 2004, 88:601-612.
59. Altintas M.M., Eddy C.K., Zhang M., McMillan J.D., Kompala D.S. Kinetic modeling to optimize pentose fermentation in Zymomonas mobilis. Biotechnol. Bioeng. 2006, 94:273-295.
60. Bruggeman F.J., Boogerd F.C., Westerhoff H.V. The multifarious short-term regulation of ammonium assimilation of Escherichia coli: dissection using an in silico replica. FEBS J. 2005, 272:1965-1985.
61. Burns K.L., Oldham C.D., Thompson J.R., Lubarsky M., May S.W. Analysis of the in vitro biocatalytic production of poly-(β)-hydroxybutyric acid. Enzyme Microb. Technol. 2007, 41:591-599.
62. Chassagnole C., Noisommit-Rizzi N., Schmid J.W., Mauch K., Reuss M. Dynamic modeling of the central carbon metabolism of Escherichia coli. Biotechnol. Bioeng. 2002, 79:53-73.
63. Hoefnagel M.H., Starrenburg M.J., Martens D.E., Hugenholtz J., Kleerebezem M., van Swam I.I., Bongers R., Westerhoff H.V., Snoep J.L. Metabolic engineering of lactic acid bacteria, the combined approach: kinetic modelling, metabolic control and experimental analysis. Microbiology 2002, 148:1003-1013.
64. Shi H., Shiraishi M., Shimizu K. Metabolic flux analysis for biosynthesis of poly(β-hydroxybutyric acid) in Alcaligenes eutrophus from various carbon sources. J. Ferment. Bioeng. 1997, 84:579-587.
65. Usuda Y., Nishio Y., Iwatani S., van Dien S.J., Imaizumi A., Shimbo K., Kageyama N., Iwahata D., Miyano H., Matsui K. Dynamic modeling of Escherichia coli metabolic and regulatory systems for amino-acid production. J. Biotechnol. 2010, 147:17-30.
66. Yang C., Hua Q., Baba T., Mori H., Shimizu K. Analysis of Escherichia coli anaplerotic metabolism and its regulation mechanisms from the metabolic responses to altered dilution rates and phosphoenolpyruvate carboxykinase knockout. Biotechnol. Bioeng. 2003, 84:129-144.
67. 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. Mol. Syst. Biol. 2009, 5:302. 10.1038/msb.2009.60.
68. Kamp A., Schuster S. Metatool 5.0: fast and flexible elementary modes analysis. Bioinformatics 2006, 22:1930-1931.
69. Katoh T., Yuguchi D., Yoshii H., Shi H., Shimizu K. Dynamics and modeling on fermentative production of poly (β-hydroxybutyric acid) from sugars via lactate by a mixed culture of Lactobacillus delbrueckii and Alcaligenes eutrophus. J. Biotechnol. 1999, 67:113-134.
70. Kayser A., Weber J., Hecht V., Rinas U. Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture. I. Growth-rate-dependent metabolic efficiency at steady state. Microbiology 2005, 151:693-706.
71. Yu J., Si Y. Metabolic carbon fluxes and biosynthesis of polyhydroxyalkanoates in Ralstonia eutropha on short chain fatty acids. Biotechnol. Prog. 2004, 20:1015-1024.
72. Leonard D., Lindley N.D. Carbon and energy flux constraints in continuous cultures of Alcaligenes eutrophus grown on phenol. Microbiology 1998, 144:241-248.
73. Pinto M.A., Immanuel C.D. Sensitivity of bifurcation traits to model parameters in poly-beta-hydroxy butyrate production. ADCHEM 2006, 103-108.
74. I. Disli, A. Kremling, A. Kienle, A model based analysis of multiple steady states in continuous cell cultures, in: Proceedings MATHMOD 09 Vienna-Full Papers CD Volume, 2009.
75. Mantzaris N.V., Kelly A.S., Daoutidis P., Srienc F. An optimal carbon source switching strategy for the production of PHA di-block copolymers with Ralstonia eutropha. A.I.Ch.E. J. 2001, 47:727-743.
76. Mantzaris N.V., Kelly A.S., Daoutidis P., Srienc F. A population balance model describing the dynamics of molecular weight distributions and the structure of PHA copolymer chains. Chem. Eng. Sci. 2002, 57:4643-4663.