Metabolic energy-based modelling explains product yielding in anaerobic mixed culture fermentations

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  González Cabaleiro, Rebeca ^a   Lema, Juan M ^a   Rodríguez, Jorge ^b  

^a UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

^b KHALIFA UNIVERSITY   (United Arab Emirates)

Author keywords

[No Author keywords available]

Indexed keywords

ACETIC ACID; ADENOSINE TRIPHOSPHATE; ALCOHOL; BUTYRIC ACID; FERREDOXIN; FORMIC ACID; PROPIONIC ACID; FORMIC ACID DERIVATIVE; GLUCOSE; HYDROGEN;

ACTIVE TRANSPORT; ANAEROBIC FERMENTATION; ARTICLE; DECARBOXYLATION; ENERGY COST; ENERGY YIELD; GLUCOSE HOMEOSTASIS; GLYCOLYSIS; MEMBRANE POTENTIAL; PH; PHOSPHORYLATION; PREDICTION; PROTON TRANSPORT; THERMODYNAMICS; VALIDATION PROCESS; ANAEROBIC GROWTH; BIOLOGICAL MODEL; BIOREACTOR; BIOREMEDIATION; ELECTRON TRANSPORT; FERMENTATION; KINETICS; METABOLISM; MICROBIOLOGY;

ANAEROBIOSIS; BIODEGRADATION, ENVIRONMENTAL; BIOLOGICAL TRANSPORT, ACTIVE; BIOREACTORS; ELECTRON TRANSPORT; FERMENTATION; FORMATES; GLUCOSE; HYDROGEN; HYDROGEN-ION CONCENTRATION; KINETICS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL;

EID: 84930672078     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126739     Document Type: Article

References (74)

1. Agler MT, Wrenn BA, Zinder SH, Angenent LT. Waste to bioproduct conversion with undefined mixed cultures: the carboxylate platform. Trends Biotechnol. 2011; 29:70-8. doi: 10.1016/j.tibtech.2010.11. 006 PMID: 21190748
2. Angenent LT, Wrenn BA. Optimizing mixed-culture bioprocessing to convert wastes into bioenergy. In: Press A, editor. Bioenergy. Washington 2008. p. 181-94.
3. Reis MA, Serafim LS, Lemos PC, Ramos AM, Aguiar FR, van Loosdrecht MCM. Production of polyhydroxyalkanoates by mixed microbial cultures. Bioprocess Biosyst Eng. 2003; 25(6):377-85. PMID: 13680343
4. Angenent LT, Karim K, Al-Dahhan MH, Wrenn BA, Domíguez-Espinosa R. Production of bioenergy and biochemicals from industrial and agricultural wastewater. Trends Biotechnol. 2004; 22(9):477-85. PMID: 15331229
5. Kleerebezem R, van Loosdrecht MCM. Mixed culture biotechnology for bioenergy production. Curr Opin Biotechnol. 2007; 18(3):207-12. PMID: 17509864
6. Eggeman T, Verser D. Recovery of Organic Acids from Fermentation Broths. In: Davison B, Evans B, Finkelstein M, McMillan J, editors. Twenty-Sixth Symposium on Biotechnology for Fuels and Chemicals. ABAB Symposium: Humana Press; 2005. p. 605-18.
7. Dellomonaco C, Clomburg JM, Miller EN, Gonzalez R. Engineered reversal of the [bgr]-oxidation cycle for the synthesis of fuels and chemicals. Nature. 2011; 476(7360):355-9. doi: 10.1038/nature10333 PMID: 21832992
8. Singhania RR, Patel AK, Christophe G, Fontanille P, Larroche C. Biological upgrading of volatile fatty acids, key intermediates for the valorization of biowaste through dark anaerobic fermentation. Bioresour Technol. 2013; 145(0):166-74.
9. Lengeler JW, Gerhart D, Schlegel HG, Georg TV. Biology of the Prokariotes. Thieme, editor. Stuttgart1999.
10. Temudo MF. Directing product formation by mixed culture fermentation. Delft: T. U. Delft; 2008.
11. Temudo MF, Kleerebezem R, van Loosdrecht MCM. Influence of the pH on (open) Mixed Culture Fermentation of Glucose: A Chemostat Study. Biotechnol Bioeng. 2007; 98(1):69-79. PMID: 17657773
12. Sieuwerts S, de Bok FAM, Hugenholtz J, van Hylckama Vlieg JET. Unraveling Microbial Interactions in Food Fermentations: from Classical to Genomics Approaches. Appl Environ Microbiol. 2008; 74(16):4997-5007. doi: 10.1128/AEM.00113-08 PMID: 18567682
13. Hoelzle RD, Virdis B, Batstone DJ. Regulation mechanisms in mixed and pure culture microbial fermentation. Biotechnol Bioeng. 2014; 111(11):2139-54. doi: 10.1002/bit.25321 PMID: 24980940
14. Jackson BE, McInerney MJ. Anaerobic microbial metabolism can proceed close to thermodynamic limits. Nature. 2002; 415(6870):454-6. PMID: 11807560
15. Smith DP, McCarty PL. Reduced product formation following perturbation of ethanol- and propionatefed methanogenic CSTRs. Biotechnol Bioeng. 1989; 34(7):885-95. PMID: 18588179
16. Kohn RA, Boston RC. The role of thermodynamics in controlling rumen metabolism. In: McNamara JP, France J, Beever DE, editors. Modelling nutrient utilization in farm animals: Oxford RU: CAB International; 2000. p. 11-21.
17. Kleerebezem R, Stams AJM. Kinetics of syntrophic cultures: a theoretical treatise on butyrate fermentation. Biotechnol Bioeng. 2000; 67(5):529-43. PMID: 10649228
18. Jin Q, Bethke CM. The thermodynamics and kinetics of microbial metabolism. Am J Sci. 2007; 307:643-77.
19. LaRowe DE, Dale AW, Amend JP, Van Cappellen P. Thermodynamic limitations on microbially catalyzed reaction rates. Geochim Cosmochim Acta. 2012; 90(0):96-109.
20. Vallino JJ. Modeling Microbial Consortiums as Distributed Metabolic Networks. Biol Bull. 2003; 204(2):174-9. PMID: 12700149
21. Gonzalez-Cabaleiro R, Lema JM, Rodriguez J, Kleerebezem R. Linking thermodynamics and kinetics to assess pathway reversibility in anaerobic bioprocesses. Energy Environ Sci. 2013; 6(12):3780-9.
22. Hoehler TM, Jorgensen BB. Microbial life under extreme energy limitation. Nat Rev Micro. 2013; 11(2):83-94.
23. Mosey FE, Matter O. Mathematical modelling of the anaerobic digestion process: Regulatory mechanisms for the formation of short-chain volatile acids from glucose. Water Sci Technol. 1983; 15(8-9):209-32.
24. Rodríguez J, Kleerebezem R, Lema JM, van Loosdrecht MCM. Modeling product formation in anaerobic mixed culture fermentations. Biotechnol Bioeng. 2006; 93(3):592-606. PMID: 16273553
25. Kleerebezem R, Rodríguez J, Temudo MF, van Loosdrecht MCM. Modeling mixed culture fermentations; the role of different electron carriers. Water Sci Technol. 2008; 57(4):493-7. doi: 10.2166/wst. 2008.094 PMID: 18359986
26. Aceves-Lara CA, Latrille E, Bernet N, Buffière P, Steyer JP. A pseudo-stoichiometric dynamic model of anaerobic hydrogen production from molasses. Water Res. 2008; 42:2539-50. doi: 10.1016/j.watres.2008.02.018 PMID: 18359057
27. Zhang F, Zhang Y, Chen M, van Loosdrecht MCM, Zeng RJ. A modified metabolic model for mixed culture fermentation with energy conserving electron bifurcation reaction and metabolite transport energy. Biotechnol Bioeng. 2013; 110(7):1884-94. doi: 10.1002/bit.24855 PMID: 23381671
28. Kleerebezem R, van Loosdrecht MCM. Critical analysis of some concepts proposed in ADM1. Water Sci Technol. 2006; 54(4):51-7. PMID: 17037169
29. Gadhamshetty V, Arudchelvam Y, Nirmalakhandan N, Johnson DC. Modeling dark fermentation for biohydrogen production: ADM1-based model vs. Gompertz model. Int J Hydrogen Energy. 2010; 35(2):479-90.
30. Batstone DJ, Keller J, Steyer JP. A review of ADM1 extensions, applications, and analysis: 2002-2005. Water Sci Technol. 2006; 54(4):1-10. PMID: 17037164
31. McCarty PL, Mosey FE. Modelling of anaerobic digestion processes (a discussion of concepts). Water Sci Technol. 1991; 24(8):17-33.
32. Lee H-S, Krajmalinik-Brown R, Zhang H, Rittmann BE. An electron-flow model can predict complex redox reactions in mixed-culture fermentative BioH2: Microbial ecology evidence. Biotechnol Bioeng. 2009; 104(4):687-97. doi: 10.1002/bit.22442 PMID: 19530077
33. Penumathsa BKV, Premier GC, Kyazze G, Dinsdale R, Guwy AJ, Esteves S, et al. ADM1 can be applied to continuous bio-hydrogen production using a variable stoichiometry approach. Water Res. 2008; 42(16):4379-85. doi: 10.1016/j.watres.2008.07.030 PMID: 18757074
34. Wu L, Wang W, van Winden WA, van Gulik WM, Heijnen JJ. A new framework for the estimation of control parameters in metabolic pathways using lin-log kinetics. Eur J Biochem. 2004; 271(16):3348-59. PMID: 15291812
35. Zoetemeyer RJ, Vandenheuvel JC, Cohen A. pH influence in acidogenic dissimilation of glucose in an anaerobic digester. Water Res. 1982; 16(3):303-11.
36. Horiuchi JI, Shimizu T, Tada K, Kanno T, Kobayashi M. Selective production of organic acids in anaerobic acid reactor by pH control. Bioresour Technol. 2002; 82(3):209-13. PMID: 11991067
37. Fang HHP, Liu H. Effect of pH on hydrogen production from glucose by a mixed culture. Bioresour Technol. 2002; 82(1):87-93. PMID: 11858207
38. Rodríguez J, Lema JM, Kleerebezem R. Energy-based models for environmental biotechnology. Trends Biotechnol. 2008; 26(7):366-74. doi: 10.1016/j.tibtech.2008.04.003 PMID: 18513813
39. Rodríguez J, Premier GC, Guwy AJ, Dinsdale R, Kleerebezem R. Metabolic models to investigate energy limited anaerobic ecosystems. Water Sci Technol. 2009; 60(7):1669-75. doi: 10.2166/wst.2009.224 PMID: 19809129
40. Papoutsakis ET, Meyer CL. Fermentation equations for propionic-acid bacteria and production of assorted oxychemicals from various sugars. Biotechnol Bioeng. 1985; 27(1):67-80. PMID: 18553577
41. Bennett GN, Rudolph FB. The central metabolic pathway from acetyl-CoA to butyryl-CoA in Clostridium acetobutylicum. FEMS Microbiol Rev. 1995; 17:241-9.
42. Schink B. Energetics of syntrophic cooperation in methanogenic degradation Microbiol Mol Biol Rev. 1997; 61(2):262-80. PMID: 9184013
43. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000; 28:27-30. PMID: 10592173
44. White D. The physiology and biochemistry of prokaryotes. Third edit ed. New York: Oxford University Press; 2007.
45. Schomburg I, Chang A, Placzek S, Söhngen C, Rother M, Lang M, et al. BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA. Nucleic Acids Res. 2013; 41(D1):D764-D72. doi: 10.1093/nar/gks1049 PMID: 23203881
46. Bar-Even A, Noor E, Flamholz A, Buescher JM, Milo R. Hydrophobicity and charge shape cellular metabolite concentrations. PLoS Comp Biol. 2011; 7:e1002166. doi: 10.1371/journal.pcbi.1002166 PMID: 21998563
47. Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, Rabinowitz JD. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol. 2009; 5(8):593-9. doi: 10.1038/nchembio.186 PMID: 19561621
48. Bar-Even A, Flamholz A, Noor E, Milo R. Thermodynamic constraints shape the structure of carbon fixation pathways. Biochim Biophys Acta. 2012; 1817(9):1646-59. doi: 10.1016/j.bbabio.2012.05.002 PMID: 22609686
49. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 1961; 191:144-8. PMID: 13771349
50. Orth JD, Thiele I, Palsson BØ. What is flux balance analysis? Nat Biotechnol. 2010; 28(3):245-8. doi: 10.1038/nbt.1614 PMID: 20212490
51. Noor E, Bar-Even A, Flamholz A, Reznik E, Liebermeister W, Milo R. Pathway Thermodynamics Highlights Kinetic Obstacles in Central Metabolism. PLoS Comput Biol. 2014; 10(2):e1003483. doi: 10.1371/journal.pcbi.1003483 PMID: 24586134
52. Heijnen JJ, Kleerebezem R. Bioenergetics of microbial growth. Encyclopedia of Industrial Biotechnology: Bioprocess, Bioseparation and Cell Technology2010. p. 1-24.
53. Thauer RK, Jungermann K, Decker K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev. 1977; 41(1):809.
54. Elston T, Wang H, Oster G. Energy transduction in ATP synthase. Nature. 1998; 391(6666):510-3. PMID: 9461222
55. ten Brink B, Otto R, Hansen UP, Konings WN. Energy recycling by lactate efflux in growing and nongrowing cells of Streptococcus cremoris. J Bacteriol. 1985; 162(1):383-90. PMID: 2984179
56. Flamholz A, Noor E, Bar-Even A, Milo R. eQuilibrator - the biochemical thermodynamics calculator. Nucleic Acids Res. 2012; 40:D770-D5. doi: 10.1093/nar/gkr874 PMID: 22064852
57. Canelas AB, van Gulik WM, Heijnen JJ. Determination of the cytosolic free NAD/NADH ratio in Saccharomyces cerevisiae under steady-state and highly dynamic conditions. Biotechnol Bioeng. 2008; 100:734-43. doi: 10.1002/bit.21813 PMID: 18383140
58. Seedorf H, Fricke WF, Veith B, Brüggemann H, Liesegang H, Strittmatter A, et al. The genome of Clostridium kluyveri, a strict anaerobe with unique metabolic features. Proc Natl Acad Sci U S A. 2008; 105(6):2128-33. doi: 10.1073/pnas.0711093105 PMID: 18218779
59. Huang H, Wang S, Moll J, Thauer RK. Electron bifurcation involved in the energy metabolism of the acetogenic bacterium Moorella thermoacetica growing on glucose or H2 plus CO2. J Bacteriol. 2012; 194(14):3689-99. doi: 10.1128/JB.00385-12 PMID: 22582275
60. Sapra R, Bagramyan K, Adams MWW. A simple energy-conserving system: proton reduction coupled to proton translocation. Proc Natl Acad Sci U S A. 2003; 100(13):7545-50. PMID: 12792025
61. Chowdhury NP, Mowafy AM, Demmer JK, Upadhyay V, Koelzer S, Jayamani E, et al. Studies on the mechanism of electron bifurcation catalyzed by electron transferring flavoprotein (Etf) and butyryl-CoA dehydrogenase (Bcd) of Acidaminococcus fermentans. J Biol Chem. 2014; 289(8):5145-57. doi: 10.1074/jbc.M113.521013 PMID: 24379410
62. Brill WJ, Wolfe RS. Ferredoxin reduction by acetaldehyde. Fed Proc. 1965; 24(2P1):233-6.
63. Yang Y-T, Bennett GN, San K-Y. The Effects of Feed and Intracellular Pyruvate Levels on the Redistribution of Metabolic Fluxes in Escherichia coli. Metab Eng. 2001; 3(2):115-23. PMID: 11289788
64. Konings W, Lolkema J, Poolman B. The generation of metabolic energy by solute transport. Arch Microbiol. 1995; 164(4):235-42.
65. Otto R, Sonnenberg AS, Veldkamp H, Konings WN. Generation of an electrochemical proton gradient in Streptococcus cremoris by lactate efflux. Proc Natl Acad Sci U S A. 1980; 77(9):5502-6. PMID: 6254084
66. von Stockar U, Maskow T, Liu J, Marison IW, Patiño R. Thermodynamics of microbial growth and metabolism: An analysis of the current situation. J Biotechnol. 2006; 121(4):517-33. PMID: 16185782
67. Kleerebezem R, van Loosdrecht MCM. A Generalized Method for Thermodynamic State Analysis of Environmental Systems. Crit Rev Environ Sci Technol. 2010; 40(1):1-54.
68. Russell JB, Cook GM. Energetics of bacterial growth: balance of anabolic and catabolic reactions. Microbiol Rev. 1995; 59(1):48-62. PMID: 7708012
69. Toei M, Gerle C, Nakano M, Tani K, Gyobu N, Tamakoshi M, et al. Dodecamer rotor ring defines H+/ATP ratio for ATP synthesis of prokaryotic V-ATPase from Thermus thermophilus. Proceedings of the National Academy of Sciences. 2007; 104(51):20256-61. PMID: 18077374
70. Pirt SJ. The maintenance energy of bacteria in growing cultures. Proc R Soc Lond B Biol Sci. 1965; 163(991):224-31. PMID: 4378482
71. Tijhuis L, van Loosdrecht MCM, Heijnen JJ. A thermodynamically based correlation for maintenance Gibbs energy requirements in aerobic and anaerobic chemotrophic growth. Biotechnol Bioengineer. 1993; 42(4):509-19. PMID: 18613056
72. Temudo MF, Muyzer G, Kleerebezem R, van Loosdrecht MC. Diversity of microbial communities in open mixed culture fermentations: impact of the pH and carbon source. Appl Microbiol Biotechnol. 2008; 80(6):1121-30. doi: 10.1007/s00253-008-1669-x PMID: 18800185
73. Diez-Gonzalez F, Russell JB. The ability of Escherichia coli 0157: H7 to decrease its intracellular pH and resist the toxicity of acetic acid. Microbiology. 1997; 143(4):1175-80.
74. Stams AJM. Metabolic interactions between anaerobic bacteria in methanogenic environments. A van Leeuw J Microb. 1994; 66(1-3):271-94.