Model-driven elucidation of the inherent capacity of Geobacter sulfurreducens for electricity generation

Journal of Biological Engineering

Volumn 7, Issue 1, 2013, Pages

  Mao, Longfei ^a   Verwoerd, Wynand S ^a  

^a LINCOLN UNIVERSITY   (New Zealand)

Author keywords

Bioelectricity; FATMIN; Flux balance analysis; Flux minimization; Flux variability analysis; Geobacter sulfurreducens; MFC; Microbial fuel cell

Indexed keywords

REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE;

ANALYSIS; ARTICLE; BACTERIAL METABOLISM; CONTROLLED STUDY; ELECTRICITY; FLUX BALANCE ANALYSIS; GENOME; GEOBACTER SULFURREDUCENS; NONHUMAN; NUTRIENT UPTAKE; PRIORITY JOURNAL; STOICHIOMETRY;

GEOBACTER SULFURREDUCENS;

EID: 84878254630     PISSN: None     EISSN: 17541611     Source Type: Journal    
DOI: 10.1186/1754-1611-7-14     Document Type: Article

References (78)

1. Caccavo F, Lonergan DJ, Lovley DR, Davis M, Stolz JF, McInerney MJ. Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing micro organism. Appl Environ Microbiol 1994, 60:3752-3759.
2. Nevin KP, Kim BC, Glaven RH, Johnson JP, Woodard TL, Methe BA, Didonato RJ, Covalla SF, Franks AE, Liu A, Lovley DR. Anode biofilm transcriptomics reveals outer surface components essential for high density current production in Geobacter sulfurreducens fuel cells. PLoS One 2009, 4:e5628.
3. Bond DR, Lovley DR. Electricity production by geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 2003, 69:1548-1555.
4. Nevin KP, Lovley DR. Mechanisms for accessing insoluble Fe(III) oxide during dissimilatory Fe(III) reduction by Geothrix fermentans. Appl Environ Microbiol 2002, 68:2294-2299.
5. Straub KL, Schink B. Evaluation of electron-shuttling compounds in microbial ferric iron reduction. FEMS Microbiol Lett 2003, 220:229-233.
6. Schröder U. Anodic electron transfer mechanisms in microbial fuel cells and their energy efficiency. Phys Chem Chem Phys 2007, 9:2619-2629.
7. Kim BH, Park HS, Kim HJ, Kim GT, Chang IS, Lee J, Phung NT. Enrichment of microbial community generating electricity using a fuel-cell-type electrochemical cell. Appl Microbiol Biotechnology 2004, 63:672-681.
8. Du Z, Li H, Gu T. A state of the art review on microbial fuel cells: a promising technology for wastewater treatment and bio energy. Biotechnol Adv 2007, 25:464-482.
9. Wang K, Liu Y, Chen S. Improved microbial electro catalysis with neutral red immobilized electrode. J Power Sources 2011, 196:164-168.
10. Rabaey K, Verstraete W. Microbial fuel cells: Novel biotechnology for energy generation. Trends Biotechnol 2005, 23:291-298.
11. Rosenbaum M, Schröder U. Photo microbial solar and fuel cells. Electro analysis 2010, 22:844-855.
12. Yang Y, Xu M, Guo J, Sun G. Bacterial extracellular electron transfer in bio electrochemical systems. Process Biochem 2012, 47:1707-1714.
13. Babanova S, Hubenova Y, Mitov M. Influence of artificial mediators on yeast-based fuel cell performance. J Biosci Bioeng 2011, 112:379-387.
14. McKinlay JB, Zeikus JG. Extracellular iron reduction is mediated in part by neutral red and hydrogenase in Escherichia coli. Appl Environ Microbiol 2004, 70:3467-3474.
15. Park DH, Zeikus JG. Electricity generation in microbial fuel cells using neutral red as an electronophore. Appl Environ Microbiol 2000, 66:1292-1297.
16. Logan BE. Exoelectrogenic bacteria that power microbial fuel cells. Nat Rev Micro 2009, 7:375-381.
17. Feist AM, Palsson BO. The biomass objective function. Curr Opin Micro bio 2010, 13:344-349.
18. Yeung M, Thiele I, Palsson B. Estimation of the number of extreme pathways for metabolic networks. BMC Bioinforma 2007, 8:363.
19. Galushko AS, Schink B. Oxidation of acetate through reactions of the citric acid cycle by Geobacter sulfurreducens in pure culture and in syntrophic coculture. Arch Microbiol 2000, 174:314-321.
20. Terzer M, Stelling J. Large-scale computation of elementary flux modes with bit pattern trees. Bioinformatics 2008, 24:2229-2235.
21. Esteve-Nunez A, Rothermich M, Sharma M, Lovley D. Growth of Geobacter sulfurreducens under nutrient-limiting conditions in continuous culture. Environ Micro bio 2005, 7:641-648.
22. Lovley DR. Extracellular electron transfer: wires, capacitors, iron lungs, and more. Geobiology 2008, 6:225-231.
23. Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR. Extracellular electron transfer via microbial nanowires. Nature 2005, 435:1098-1101.
24. Reguera G, Nevin KP, Nicoll JS, Covalla SF, Woodard TL, Lovley DR. Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl Environ Microbiol 2006, 72:7345-7348.
25. Rabaey K, Lissens G, Siciliano SD, Verstraete W. A microbial fuel cell capable of converting glucose to electricity at high rate and efficiency. Biotechnol Lett 2003, 25:1531-1535.
26. Nevin KP, Richter H, Covalla SF, Johnson JP, Woodard TL, Orloff AL, Jia H, Zhang M, Lovley DR. Power output and columbic efficiencies from biofilms of Geobacter sulfurreducens comparable to mixed community microbial fuel cells. Environ Microbiol 2008, 10:2505-2514.
27. Yi H, Nevin KP, Kim BC, Franks AE, Klimes A, Tender LM, Lovley DR. Selection of a variant of Geobacter sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens Bio electron 2009, 24:3498-3503.
28. Lovley DR. Microbial fuel cells: novel microbial physiologies and engineering approaches. Curr Opin Biotechnol 2006, 17:327-332.
29. Lovley DR. Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 2006, 4:497-508.
30. Stewart PS, Franklin MJ. Physiological heterogeneity in biofilms. Nat Rev Micro 2008, 6:199-210.
31. Mahadevan R, Bond DR, Butler JE, Esteve-Nunez A, Coppi MV, Palsson BO, Schilling CH, Lovley DR. Characterization of metabolism in the Fe(III)-reducing organism Geobacter sulfurreducens by constraint-based modeling. Appl Environ Microbiol 2006, 72:1558-1568.
32. Lovley DR. Electro microbiology. Annu Rev Microbiol 2012, 66:391-409.
33. Pharkya P, Burgard AP, Maranas CD. Exploring the overproduction of amino acids using the bilevel optimization framework Opt Knock. Biotechnol Bioeng 2003, 84:887-899.
34. Reed J, Vo T, Schilling C, Palsson B. An expanded genome-scale model of Escherichia coli K-12 (iJR904 GSM/GPR). Genome Biol 2003, 4:R54.
35. Burgard AP, Maranas CD. Optimization-based framework for inferring and testing hypothesized metabolic objective functions. Biotechnology Bioeng 2003, 82:670-677.
36. Rocha M, Maia P, Mendes R, Pinto JP, Ferreira EC, Nielsen J, Patil KR, Rocha I. Natural computation meta-heuristics for the in silico optimization of microbial strains. BMC Bioinforma 2008, 9:499.
37. Patil K, Rocha I, Forster J, Nielsen J. Evolutionary programming as a platform for in silico metabolic engineering. BMC Bioinforma 2005, 6:308.
38. Lee K, Berthiaume F, Stephanopoulos GN, Yarmush DM, Yarmush ML. Metabolic flux analysis of post burn hepatic hyper metabolism. Metab Eng 2000, 2:312-327.
39. Mahadevan R, Schilling CH. The effects of alternate optimal solutions in constraint-based genome-scale metabolic models. Metab Eng 2003, 5:264-276.
40. Reed JL, Palsson B. Genome-scale in silico models of E. coli have multiple equivalent phenotypic states: assessment of correlated reaction subsets that comprise network states. Genome Res 2004, 14:1797-1805.
41. Thiele I, Fleming RMT, Bordbar A, Schellenberger J, Palsson B. Functional characterization of alternate optimal solutions of Escherichia coli's transcriptional and translational machinery. Biophys J 2010, 98:2072-2081.
42. Price ND, Famili I, Beard DA, Palsson BO. Extreme pathways and Kirchhoff's second law. Biophys J 2002, 83:2879-2882.
43. Schuster S, Hilgetag C. On elementary flux modes in biochemical reaction systems at steady state. J Biol Syst 1994, 2:165-182.
44. Duarte N, Herrgard M, Palsson B. Reconstruction and validation of Saccharomyces cerevisiae iND750, a fully compartmentalized genome-scale metabolic model. Genome Res 2004, 14:1298-1309.
45. Beard DA, Liang SD, Qian H. Energy balance for analysis of complex metabolic networks. Biophys J 2002, 83:79-86.
46. Varma A, Palsson BO. Metabolic capabilities of Escherichia coli: I. synthesis of biosynthetic precursors and cofactors. J Theor Biol 1993, 165:477-502.
47. Holzhütter HG. The principle of flux minimization and its application to estimate stationary fluxes in metabolic networks. Eur J Biochem 2004, 271:2905-2922.
48. Henry CS, Broadbelt LJ, Hatzimanikatis V. Thermodynamics-based metabolic flux analysis. Biophys J 2007, 92:1792-1805.
49. Fleming RMT, Thiele I, Provan G, Nasheuer HP. Integrated stoichiometric, thermodynamic and kinetic modelling of steady state metabolism. J Theor Biol 2010, 264:683-692.
50. Fleming RMT, Thiele I. von Bertalanffy 1.0: a COBRA toolbox extension to thermodynamically constrain metabolic models. Bioinformatics 2011, 27:142-143.
51. Cogne G, Rügen M, Bockmayr A, Titica M, Dussap C-G, Cornet J-F, Legrand J. A model-based method for investigating bioenergetic processes in autotrophically growing eukaryotic microalgae: Application to the green algae Chlamydomonas reinhardtii. Biotechnol Prog 2011, 27:631-640.
52. Noor E, Bar-Even A, Flamholz A, Lubling Y, Davidi D, Milo R. An integrated open framework for thermodynamics of reactions that combines accuracy and coverage. Bioinformatics 2012, 28:2037-2044.
53. De Martino D, Figliuzzi M, De Martino A, Marinari E. A scalable algorithm to explore the Gibbs energy landscape of genome-scale metabolic networks. PLoS Comput Biol 2012, 8:e1002562.
54. Beard DA, Qian H. Thermodynamic-based computational profiling of cellular regulatory control in hepatocyte metabolism. Am J Physiol Endocrinol Metab 2005, 288:E633-E644.
55. Lewis NE, Hixson KK, Conrad TM, Lerman JA, Charusanti P, Polpitiya AD, Adkins JN, Schramm G, Purvine SO, Lopez-Ferrer D. Omic data from evolved E. coli are consistent with computed optimal growth from genome-scale models. Mol Syst Biol 2010, 6:390.
56. Schuetz R, Zamboni N, Zampieri M, Heinemann M, Sauer U. Multidimensional optimality of microbial metabolism. Science 2012, 336:601-604.
57. Klitgord N, Segrè D. The importance of compartmentalization in metabolic flux models: yeast as an ecosystem of organelles. Genome Inform 2010, 22:41-55.
58. Kelk SM, Olivier BG, Stougie L, Bruggeman FJ. Optimal flux spaces of genome-scale stoichiometric models are determined by a few subnetworks. Sci Rep 2012, 2:580.
59. Park DH, Kim SK, Shin IH, Jeong YJ. Electricity production in bio fuel cell using modified graphite electrode with Neutral Red. Biotechnol Lett 2000, 22:1301-1304.
60. Boyle NR, Morgan JA. Flux balance analysis of primary metabolism in Chlamydomonas reinhardtii. BMC Syst Biol 2009, 3:4.
61. Shastri AA, Morgan JA. Flux balance analysis of photoautotrophic metabolism. Biotechnol Prog 2005, 21:1617-1626.
62. Aklujkar M, Coppi MV, Leang C, Kim BC, Chavan MA, Perpetua LA, Giloteaux L, Liu A, Holmes D. Proteins involved in electron transfer to Fe(III) and Mn(IV) oxides by Geobacter sulfurreducens and Geobacter uraniireducens. Microbiology 2013, 159:515-535.
63. Sun J, Sayyar B, Butler JE, Pharkya P, Fahland TR, Famili I, Schilling CH, Lovley DR, Mahadevan R. Genome-scale constraint-based modeling of Geobacter metallireducens. BMC Syst Biol 2009, 3:15.
64. Kim K-Y, Chae K-J, Choi M-J, Ajayi FF, Jang A, Kim C-W, Kim IS. Enhanced coulombic efficiency in glucose-fed microbial fuel cells by reducing metabolite electron losses using dual-anode electrodes. Bioresour Technol 2011, 102:4144-4149.
65. Logan BE, Hamelers B, Rozendal R, Schröder U, Keller J, Freguia S, Aelterman P, Verstraete W, Rabaey K. Microbial fuel cells: methodology and technology. Environ Sci Technol 2006, 40:5181-5192.
66. Virdis B, Freguia S, Rozendal RA, Rabaey K, Yuan Z, Keller J. 4.18 - Microbial Fuel Cells. Treatise on Water Science 2011, 641-666. Oxford: Elsevier, Peter W.
67. Cheng S, Liu H, Logan BE. Increased power generation in a continuous flow MFC with advective flow through the porous anode and reduced electrode spacing. Environ Sci Technol 2006, 40:2426-2432.
68. Zhao F, Harnisch F, Schröder U, Scholz F, Bogdanoff P, Herrmann I. Challenges and constraints of using oxygen cathodes in microbial fuel cells. Environ Sci Technol 2006, 40:5193-5199.
69. Suthers PF, Zomorrodi A, Maranas CD. Genome-scale gene/reaction essentiality and synthetic lethality analysis. Mol Syst Biol 2009, 5:301.
70. Zomorrodi A, Maranas C. Improving the iMM904 S. cerevisiae metabolic model using essentiality and synthetic lethality data. BMC Syst Biol 2010, 4:178.
71. Zhuang K, Izallalen M, Mouser P, Richter H, Risso C, Mahadevan R, Lovley DR. Genome-scale dynamic modeling of the competition between Rhodoferax and Geobacter in anoxic subsurface environments. ISME J 2011, 5:305-316.
72. Segura D, Mahadevan R, Juarez K, Lovley DR. Computational and experimental analysis of redundancy in the central metabolism of Geobacter sulfurreducens. PLoS Comput Biol 2008, 4:e36.
73. Verwoerd W. A new computational method to split large biochemical networks into coherent subnets. BMC Syst Biol 2011, 5:25.
74. Verwoerd W. Interactive extraction of metabolic subnets - the netsplitter software implementation. Journal of Molecular Engineering and Systems Biology 2012, 1:2-2.
75. Varma A, Palsson BO. Metabolic flux balancing: basic concepts, scientific and practical Use. Nat Biotech 1994, 12:994-998.
76. Orth JD, Thiele I, Palsson BO. What is flux balance analysis?. Nat Biotech 2010, 28:245-248.
77. Schellenberger J, Que R, Fleming RM, Thiele I, Orth JD, Feist AM, Zielinski DC, Bordbar A, Lewis NE, Rahmanian S. Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0. Nat Protoc 2011, 6:1290-1307.
78. Rocha I, Maia P, Evangelista P, Vilaca P, Soares S, Pinto JP, Nielsen J, Patil KR, Ferreira EC, Rocha M. OptFlux: an open-source software platform for in silico metabolic engineering. BMC Syst Biol 2010, 4:45.