Dynamic flux balance modeling of S. cerevisiae and E. coli co-cultures for efficient consumption of glucose/xylose mixtures

Applied Microbiology and Biotechnology

Volumn 93, Issue 6, 2012, Pages 2529-2541

  Hanly, Timothy J ^a   Urello, Morgan ^a   Henson, Michael A ^a  

^a University of Massachusetts   (United States)

Author keywords

Co culture; Escherichia coli; In silico; Metabolic flux analysis; Saccharomyces cerevisiae

Indexed keywords

ALTERNATIVE APPROACH; BATCH GROWTH; CELL CONCENTRATIONS; CO-CULTURES; COCULTURE; COMPLEX SUGARS; DIAUXIC GROWTH; E. COLI; EXPERIMENTAL IDENTIFICATION; EXPERIMENTAL VALIDATIONS; FLUX BALANCE; FLUX BALANCE MODEL; GROWTH CONDITIONS; IN-SILICO; INHIBITORY EFFECT; LIGNOCELLULOSIC FEEDSTOCKS; METABOLIC FLUX ANALYSIS; METABOLIC RECONSTRUCTION; MICROBIAL CONSORTIA; MODEL PREDICTION; OPTIMAL GROWTH; PROFILE PREDICTION; PURE CULTURE; S.CEREVISIAE; SUBSTRATE UPTAKE; SUGAR MIXTURES; WILD TYPES;

BACTERIA; ESCHERICHIA COLI; ETHANOL; FORECASTING; GLUCOSE; METABOLISM; MIXTURES; OPTIMIZATION; SEDIMENTATION; SUBSTRATES; YEAST;

CELL CULTURE;

DISSOLVED OXYGEN; GLUCOSE; XYLOSE;

BIOCHEMISTRY; BIOTECHNOLOGY; CELLULOSE; FECAL COLIFORM; GROWTH; LIGNIN; MICROBIAL ACTIVITY; MODEL VALIDATION; NUMERICAL MODEL; PH; RECONSTRUCTION; SUGAR; YEAST;

ALCOHOL CONSUMPTION; ANAEROBIC FERMENTATION; ANAEROBIC GROWTH; ARTICLE; BACTERIAL GROWTH; BACTERIUM CULTURE; BATCH FERMENTATION; BIOMASS PRODUCTION; CARBON SOURCE; CELL COUNT; CITRIC ACID CYCLE; COCULTURE; COMPUTER MODEL; CONTINUOUS CULTURE; ESCHERICHIA COLI; FUNGUS CULTURE; FUNGUS GROWTH; GLUCOSE INTAKE; GROWTH CURVE; GROWTH RATE; MICROBIAL CONSORTIUM; MIXED CELL CULTURE; NONHUMAN; OXYGEN CONSUMPTION; PH; SACCHAROMYCES CEREVISIAE; TEMPERATURE; AEROBIC METABOLISM; FERMENTATION; GENETICS; METABOLISM;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

AEROBIOSIS; COCULTURE TECHNIQUES; ESCHERICHIA COLI; FERMENTATION; GLUCOSE; SACCHAROMYCES CEREVISIAE; XYLOSE;

EID: 84862272463     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-011-3628-1     Document Type: Article

References (49)

1. Abbott DA, Zelle RM, Pronk JT, Van Maris AJA (2009) Metabolic engineering of Saccharomyces cerevisiae for production of carboxylic acids: Current status and challenges. FEMS Yeast Res 9(8):1123-1136. doi:10.1111/j.1567-1364.2009. 00537.x
2. Alper H, Stephanopoulos G (2009) Engineering for biofuels: Exploiting innate microbial capacity or importing biosynthetic potential? Nat Rev Micro 7(10):715-723. doi:10.1038/nrmicro2186
3. Beck M, Johnson R, Baker C (1990) Ethanol production from glucose/xylose mixes by incorporating microbes in selected fermentation schemes. Appl Biochem Biotech 24-25(1):415-424. doi:10.1007/bf02920265
4. Blank LM, Sauer U (2004) TCA cycle activity in Saccharomyces cerevisiae is a function of the environmentally determined specific growth and glucose uptake rates. Microbiology 150 :1085-1093. doi:10.1099/mic.0.26845-0
5. Brenner K, You L, Arnold FH (2008) Engineering microbial consortia: A new frontier in synthetic biology. Trends Biotechnol 26(9):483-489. doi:10.1016/j.tibtech.2008.05.004
6. Curtis SJ, Epstein W (1975) Phosphorylation of D-glucose in Escherichia coli mutants defective in glucosephosphotransferase, mannosephosphotransferase, and glucokinase. J Bacteriol 122 :1189-1199
7. Davison BH, Stephanopoulos G (1986a) Coexistence of S. cerevisiae and E. coli in chemostat under substrate competition and product inhibition. Biotechnol Bioeng 28(11):1742-1752. doi:10.1002/ bit.260281119
8. Davison BH, Stephanopoulos G (1986b) Effect of pH oscillations on a competing mixed culture. Biotechnol Bioeng 28(8):1127-1137. doi:10.1002/bit. 260280802
9. De Bari I, Cuna D, Nanna F, Braccio G (2004) Ethanol production in immobilized-cell bioreactors from mixed sugar syrups and enzymatic hydrolysates of steam-exploded biomass. Appl Biochem Biotech 114(1):539-557. doi:10.1385/abab:114:1-3:539
10. Drake JF, Tsuchiya HM (1973) Differential counting in mixed cultures with coulter counters. Appl Environ Microbiol 26(1):9-13
11. Duarte NC, Herrgård MJ, Palsson BØ (2004) Reconstruction and validation of Saccharomyces cerevisiae iND750, a fully compartmentalized genome-scale metabolic model. Genome Res 14 :1298-1309. doi:10.1101/gr.2250904
12. Echave P, Esparza-Cerón MA, Cabiscol E, Tamarit J, Ros J, Membrillo-Hernández J, Lin ECC (2002) DnaK dependence of mutant ethanol oxidoreductases evolved for aerobic function and protective role of the chaperone against protein oxidative damage in Escherichia coli. P Natl Acad Sci USA 99(7):4626-4631. doi:10.1073/pnas.072504199
13. Eiteman M, Lee S, Altman E (2008) A co-fermentation strategy to consume sugar mixtures effectively. J Biol Eng 2(1):1-8. doi:10.1186/1754-1611-2-3
14. Eiteman MA, Lee SA, Altman R, Altman E (2009) A substrateselective co-fermentation strategy with Escherichia coli produces lactate by simultaneously consuming xylose and glucose. Biotechnol Bioeng 102(3):822-827. doi:10.1002/bit.22103
15. Feist AM, Herrgard MJ, Thiele I, Reed JL, Palsson BO (2009) Reconstruction of biochemical networks in microorganisms. Nat Rev Micro 7(2):129-143. doi:10.1038/nrmicro1949
16. Fong SS, Burgard AP, Herring CD, Knight EM, Blattner FR, Maranas CD, Palsson BO (2005) In silico design and adaptive evolution of Escherichia coli for production of lactic acid. Biotechnol Bioeng 91(5):643-648. doi:10.1002/bit.20542
17. Govindaswamy S, Vane LM (2007) Kinetics of growth and ethanol production on different carbon substrates using genetically engineered xylose-fermenting yeast. Bioresour Technol 98 :677-685. doi:10.1016/j.biortech.2006.02.012
18. Guijarro JM, Lagunas R (1984) Saccharomyces cerevisiae does not accumulate ethanol against a concentration gradient. J Bacteriol 160(3):874-878
19. Hanly TJ, Henson MA (2011) Dynamic flux balance modeling of microbial co-cultures for efficient batch fermentation of glucose and xylose mixtures. Biotechnol Bioeng 108(2):376-385. doi:10.1002/bit.22954
20. Hjersted JL, Henson MA (2006) Optimization of fed-batch Saccharomyces cerevisiae fermentation using dynamic flux balance models. Biotechnol Progr 22(5):1239-1248. doi:10.1021/ bp060059v
21. Hjersted JL, Henson MA (2009) Steady-state and dynamic flux balance analysis of ethanol production by Saccharomyces cerevisiae. IET Syst Bio 3(3):167-179. doi:10.1049/ietsyb. 2008.0103
22. Hjersted JL, Henson MA, Mahadevan R (2007) Genome-scale analysis of Saccharomyces cerevisiae metabolism and ethanol production in fed-batch culture. Biotechnol Bioeng 97(5):1190-1204. doi:10.1002/bit.21332
23. Klitgord N, Segrè D (2010) Environments that induce synthetic microbial ecosystems. PLoS Comput Biol 6(11):e1001002. doi:10.1371/journal.pcbi. 1001002
24. Laplace JM, Delgenes JP, Moletta R, Navarro JM (1993) Ethanol production from glucose and xylose by separated and co-culture processes using high cell density systems. Process Biochem 28 :519-525. doi:10.1016/0032-9592(93)85013-6
25. Lawford H, Rousseau J (1994) Relative rates of sugar utilization by an ethanologenic recombinant Escherichia coli using mixtures of glucose, mannose, and xylose. Appl Biochem Biotech 45-46 :367-381. doi:10.1007/bf02941812
26. Lee SK, Chou H, Ham TS, Lee TS, Keasling JD (2008) Metabolic engineering of microorganisms for biofuels production: From bugs to synthetic biology to fuels. Curr Opin Biotech 19(6):556-563. doi:10.1016/j.copbio.2008.10.014
27. Leschine S, Canale-Parola E (1984) Ethanol production from cellulose by a coculture of Zymomonas mobilis and a clostridium. Curr Microbiol 11(3):129-135. doi:10.1007/bf01567337
28. Mahadevan R, Edwards JS, Doyle Iii FJ (2002) Dynamic flux balance analysis of diauxic growth in Escherichia coli. Biophys J 83 1331-1340. doi:10.1016/S0006-3495(02)73903-9
29. Meadows AL, Karnik R, Lam H, Forestell S, Snedecor B (2010) Application of dynamic flux balance analysis to an industrial Escherichia coli fermentation. Metab Eng 12(2):150-160. doi:10.1016/j.ymben.2009.07.006
30. Ohta K, Beall DS, Mejia JP, Shanmugam KT, Ingram LO (1991) Genetic improvement of Escherichia coli for ethanol production: Chromosomal integration of Zymomonas mobilis genes encoding pyruvate decarboxylase and alcohol dehydrogenase II. Appl Environ Microbiol 57(4):893-900
31. Okuda N, Ninomiya K, Katakura Y, Shioya S (2008) Strategies for reducing supplemental medium cost in bioethanol production from waste house wood hydrolysate by ethanologenic Escherichia coli: Inoculum size increase and coculture with Saccharo-myces cerevisiae. J Biosci Bioeng 105(2):90-96. doi:10.1263/ jbb.105.90
32. Price ND, Papin JA, Schilling CH, Palsson BO (2003) Genome-scale microbial in silico models: The constraints-based approach. Trends Biotechnol 21(4):162-169. doi:10.1016/S0167-7799(03) 00030-1
33. Qian M, Tian S, Li X, Zhang J, Pan Y, Yang X (2006) Ethanol production from dilute-acid softwood hydrolysate by co-culture. Appl Biochem Biotech 134(3):273-283. doi:10.1385/ ABAB:134:3:273
34. Reed J, Vo T, Schilling C, Palsson B (2003) An expanded genomescale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biol 4(9):R54. doi:10.1186/gb-2003-4-9-r54
35. Rieger M, Kappeli O, Fiechter A (1983) The role of limited respiration in the incomplete oxidation of glucose by Saccharomyces cerevisiae. J Gen Microbiol 129(3):653-661. doi:10.1099/ 00221287-129-3-653
36. Saerens S, Duong C, Nevoigt E (2010) Genetic improvement of brewer's yeast: Current state, perspectives and limits. ApplMicrobiol Biot 86 :1195-1212. doi:10.1007/s00253-010-2486-6
37. Salimi F, Zhuang K, Mahadevan R (2010) Genome-scale metabolic modeling of a clostridial co-culture for consolidated bioprocessing. Biotech J 5(7):726-738. doi:10.1002/biot.201000159
38. Sedlak M, Edenberg HJ, Ho NWY (2003) DNA microarray analysis of the expression of the genes encoding the major enzymes in ethanol production during glucose and xylose co-fermentation by metabolically engineered Saccharomyces yeast. Enz Microbiol Technol 33(1):19-28. doi:10.1016/S0141-0229(03)00067-X
39. Senger RS (2010) Biofuel production improvement with genomescale models: The role of cell composition. Biotechnol J 5:671-685. doi:10.1002/biot.201000007
40. Senger RS, Papoutsakis ET (2008) Genome-scale model for Clostridium acetobutylicum: Part II. Development of specific proton flux states and numerically determined sub-systems. Biotechnol Bioeng 101(5):1053-1071. doi:10.1002/bit.22009
41. Sonnleitner B, Käppeli O (1986) Growth of Saccharomyces cerevisiae is controlled by its limited respiratory capacity: Formulation and verification of a hypothesis. Biotechnol Bioeng 28(6):927-937. doi:10.1002/bit.260280620
42. Stolyar S, Van Dien S, Hillesland KL, Pinel N, Lie TJ, Leigh JA, Stahl DA (2007) Metabolic modeling of a mutualistic microbial community. Mol Syst Biol 3:92. doi:10.1038/msb4100131
43. Taniguchi M, Itaya T, Tohma T, Fujii M (1997a) Ethanol production from a mixture of glucose and xylose by a novel co-culture system with two fermentors and two microfiltration modules. J Ferment Bioeng 84(1):59-64. doi:10.1016/S0922-338X(97) 82787-0
44. Taniguchi M, Tohma T, Itaya T, Fujii M (1997b) Ethanol production from a mixture of glucose and xylose by co-culture of Pichia stipitis and a respiratory-deficient mutant of Saccharomyces cerevisiae. J Ferment Bioeng 83(4):364-370. doi:10.1016/ S0922-338X(97)80143-2
45. van Maris A, Abbott D, Bellissimi E, van den Brink J, Kuyper M, Luttik M, Wisselink H, Scheffers W, van Dijken J, Pronk J (2006) Alcoholic fermentation of carbon sources in biomass hydrolysates by Saccharomyces cerevisiae: Current status. Antonie van Leeuwenhoek 90(4):391-418. doi:10.1007/s10482-006-9085-7
46. van Zyl W, Lynd L, den Haan R, McBride J (2007) Consolidated bioprocessing for bioethanol production using Saccharomyces cerevisiae. Adv Biochem Eng Biotechnol 108:205-235. doi:10.1007/10-2007-061
47. Varma A, Palsson BO (1994) Stoichiometric flux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110. Appl Environ Microbiol 60 :3724-3731
48. Yomano L, York S, Zhou S, Shanmugam K, Ingram L (2008) Reengineering Escherichia coli for ethanol production. Biotechnol Lett 30(12):2097-2103. doi:10.1007/s10529-008-9821-3
49. Zhuang K, Izallalen M, Mouser P, Richter H, Risso C, Mahadevan R, Lovley DR (2010) Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments. ISME J 5(2):305-316. doi:10.1038/ ismej.2010.117