期刊论文详细信息
Biotechnology for Biofuels
Theoretical exploration of optimal metabolic flux distributions for extracellular electron transfer by Shewanella oneidensis MR-1
Longfei Mao1  Wynand S Verwoerd1 
[1] Centre for Advanced Computational Solutions, Department of Molecular Biosciences, Lincoln University, Ellesmere Junction Road/Springs Road, Lincoln 7647, Canterbury Plains, New Zealand
关键词: Microbial metabolism;    FATMIN;    Flux minimization;    Flux variability analysis;    Flux balance analysis;    Bioelectricity;    Shewanella oneidensis MR-1;    Microbial fuel cell;    MFC;   
Others  :  1084661
DOI  :  10.1186/s13068-014-0118-6
 received in 2014-04-16, accepted in 2014-07-25,  发布年份 2014
PDF
【 摘 要 】

Background

Shewanella oneidensis MR-1 is one of the model microorganisms used for extracellular electron transfer. In this study, to elucidate the capability and the relevant metabolic processes of S. oneidensis MR-1 involved in an electron transferring environment, we employed genome-scale modelling to model the necessary metabolic states and flux adjustments for electricity generation in the cytochrome c-based direct electron transfer (DET) mode, the NADH-linked mediated electron transfer (MET) mode and a presumable mixed mode comprising DET and flavin secretion. These are difficult to develop experimentally.

Results

The results showed that the microbe had the potential to achieve current outputs of up to 2.610 A/gDW in the DET mode, 2.189 A/gDW in the MET mode and 2.197 A/gDW in the mixed mode. Compared with the DET mode, which relied on cytochrome c oxidase (EC: 1.1.1.2) to mediate the electron transfer, the MET mode was mainly dependent on two routes, catalysed by isocitrate dehydrogenase (NAD) (EC: 1.1.1.4) and NAD transhydrogenase, for the computed high current density value. In the mixed mode, whereas the cytochrome c-based DET accounted for most of the computed maximum current output value, the two flavins combined, riboflavin and FMN, played a much less important role in the probed current value.

Conclusions

Shewanella oneidensis MR-1 has the potential to sustain a high extracellular electron transfer rate similarly to Geobacter sulfurreducens, but relies on different intracellular mechanisms. Various levels of electron transfer rates are achieved by different combinations of metabolic pathways. Flavins can significantly degenerate the maximum electricity generation capability of the cell and the biomass formation, and thus should be avoided in order to achieve a high coulombic efficiency.

【 授权许可】

   
2014 Mao and Verwoerd; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150113163401949.pdf 2373KB PDF download
Figure 9. 53KB Image download
Figure 8. 107KB Image download
Figure 7. 41KB Image download
Figure 6. 42KB Image download
Figure 5. 37KB Image download
Figure 4. 44KB Image download
Figure 3. 33KB Image download
Figure 2. 38KB Image download
Figure 1. 100KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

Figure 9.

【 参考文献 】
  • [1]Meshulam-Simon G, Behrens S, Choo A, Spormann A: Hydrogen metabolism in Shewanella oneidensis MR-1. Appl Environ Microbiol 2007, 73:1153-1165.
  • [2]Myers CR, Nealson KH: Bacterial manganese reduction and growth with manganese oxide as the sole electron acceptor. Science 1988, 240:1319-1321.
  • [3]Huang L, Logan B: Electricity generation and treatment of paper recycling wastewater using a microbial fuel cell. Appl Microbiol Biotechnol 2008, 80:349-355.
  • [4]Kargi F, Eker S: Electricity generation with simultaneous wastewater treatment by a microbial fuel cell (MFC) with Cu and Cu-Au electrodes. J Chem Technol Biotechnol 2007, 82:658-662.
  • [5]Brutinel E, Gralnick J: Shuttling happens: soluble flavin mediators of extracellular electron transfer in Shewanella. Appl Microbiol Biotechnol 2012, 93:41-48.
  • [6]Schröder U: Anodic electron transfer mechanisms in microbial fuel cells and their energy efficiency. Phys Chem Chem Phys 2007, 9:2619-2629.
  • [7]Mao L, Verwoerd WS: Selection of organisms for systems biology study of microbial electricity generation: a review. Int J Energy Env Eng 2013, 4:17. BioMed Central Full Text
  • [8]El-Naggar MY, Wanger G, Leung KM, Yuzvinsky TD, Southam G, Yang J, Lau WM, Nealson KH, Gorby YA: Electrical transport along bacterial nanowires from Shewanella oneidensis MR-1. Proc Natl Acad Sci U S A 2010, 107:18127-18131.
  • [9]Boesen T, Nielsen LP: Molecular dissection of bacterial nanowires. Mbio 2013, 4:e00270-13.
  • [10]Reguera G, McCarthy KD, Mehta T, Nicoll JS, Tuominen MT, Lovley DR: Extracellular electron transfer via microbial nanowires. Nature 2005, 435:1098-1101.
  • [11]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.
  • [12]Gorby YA, Yanina S, McLean JS, Rosso KM, Moyles D, Dohnalkova A, Beveridge TJ, Chang IS, Kim BH, Kim KS, Culley DE, Reed SB, Romine MF, Saffarini DA, Hill EA, Shi L, Elias DA, Kennedy DW, Pinchuk G, Watanabe K, Ishii S, Logan B, Nealson KH, Fredrickson JK: Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci U S A 2006, 103:11358-11363.
  • [13]El-Naggar MY, Gorby YA, Xia W, Nealson KH: The molecular density of states in bacterial nanowires. Biophys J 2008, 95:L10-L12.
  • [14]Lovley DR: Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 2006, 4:497-508.
  • [15]Fredrickson JK, Romine MF, Beliaev AS, Auchtung JM, Driscoll ME, Gardner TS, Nealson KH, Osterman AL, Pinchuk G, Reed JL, Rodionov DA, Rodrigues JL, Saffarini DA, Serres MH, Spormann AM, Zhulin IB, Tiedje JM: Towards environmental systems biology of Shewanella. Nat Rev Microbiol 2008, 6:592-603.
  • [16]von Canstein H, Ogawa J, Shimizu S, Lloyd JR: Secretion of flavins by Shewanella species and their role in extracellular electron transfer. Appl Environ Microbiol 2008, 74:615-623.
  • [17]Velasquez-Orta SB, Head IM, Curtis TP, Scott K, Lloyd JR, von Canstein H: The effect of flavin electron shuttles in microbial fuel cells current production. Appl Microbiol Biotechnol 2010, 85:1373-1381.
  • [18]Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR: Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci 2008, 105:3968-3973.
  • [19]Liu H, Matsuda S, Hashimoto K, Nakanishi S: Flavins secreted by bacterial cells of Shewanella catalyze cathodic oxygen reduction. Chem Sus Chem 2012, 5:1054-1058.
  • [20]Bouhenni RA, Vora GJ, Biffinger JC, Shirodkar S, Brockman K, Ray R, Wu P, Johnson BJ, Biddle EM, Marshall MJ, Fitzgerald LA, Little BJ, Fredrickson JK, Beliaey AS, Ringeisen BR, Saffarini DA: The role of Shewanella oneidensis MR-1 outer surface structures in extracellular electron transfer. Electroanalysis 2010, 22:856-864.
  • [21]Coursolle D, Baron DB, Bond DR, Gralnick JA: The Mtr respiratory pathway is essential for reducing flavins and electrodes in Shewanella oneidensis. J Bacteriol 2010, 192:467-474.
  • [22]Park DH, Zeikus JG: Electricity generation in microbial fuel cells using neutral red as an electronophore. Appl Environ Microbiol 2000, 66:1292-1297.
  • [23]Ross DE, Flynn JM, Baron DB, Gralnick JA, Bond DR: Towards electrosynthesis in Shewanella: energetics of reversing the Mtr pathway for reductive metabolism. PLoS One 2011, 6:e16649.
  • [24]Serres M, Riley M: Genomic analysis of carbon source metabolism of Shewanella oneidensis MR-1: predictions versus experiments. J Bacteriol 2006, 188:4601-4609.
  • [25]McCloskey D, Palsson BO, Feist AM: Basic and applied uses of genome-scale metabolic network reconstructions of Escherichia coli. Mol Syst Biol 2013, 9:661.
  • [26]Michelusi N, Pirbadian S, El-Naggar MY, Mitra U: A model for electron transfer and cell energetics in bacterial cables. In 2014 48th Annual Conference on Information Sciences and Systems (CISS), 19-21 March 2014. IEEE, Princeton, NJ; 2014:1-6.
  • [27]Moore MJ, Suda T, Oiwa K: Molecular communication: modeling noise effects on information rate. IEEE Trans Nanobioscience 2009, 8:169-180.
  • [28]Pirbadian S, El-Naggar MY: Multistep hopping and extracellular charge transfer in microbial redox chains. Phys Chem Chem Phys 2012, 14:13802-13808.
  • [29]Biffinger JC, Ray R, Little BJ, Fitzgerald LA, Ribbens M, Finkel SE, Ringeisen BR: Simultaneous analysis of physiological and electrical output changes in an operating microbial fuel cell with Shewanella oneidensis. Biotechnol Bioeng 2009, 103:524-531.
  • [30]Rosenbaum M, Cotta MA, Angenent LT: Aerated Shewanella oneidensis in continuously fed bioelectrochemical systems for power and hydrogen production. Biotechnol Bioeng 2010, 105:880-888.
  • [31]TerAvest MA, Rosenbaum MA, Kotloski NJ, Gralnick JA, Angenent LT: Oxygen allows Shewanella oneidensis MR-1 to overcome mediator washout in a continuously fed bioelectrochemical system. Biotechnol Bioeng 2014, 111:692-699.
  • [32]Meyer TE, Tsapin AI, Vandenberghe I, de Smet L, Frishman D, Nealson KH, Cusanovich MA, van Beeumen JJ: Identification of 42 possible cytochrome C genes in the Shewanella oneidensis genome and characterization of six soluble cytochromes. OMICS 2004, 8:57-77.
  • [33]Mao L, Verwoerd WS: Model-driven elucidation of the inherent capacity of Geobacter sulfurreducens for electricity generation. J Biol Eng 2013, 7:14. BioMed Central Full Text
  • [34]Pinchuk GE, Hill EA, Geydebrekht OV, De Ingeniis J, Zhang X, Osterman A, Scott JH, Reed SB, Romine MF, Konopka AE, Beliaev AS, Fredrickson JK, Reed JL: Constraint-based model of Shewanella oneidensis MR-1 metabolism: a tool for data analysis and hypothesis generation. PLoS Comp Biol 2010, 6:e1000822.
  • [35]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.
  • [36]Call DF, Logan BE: Lactate oxidation coupled to iron or electrode reduction by Geobacter sulfurreducens PCA. Appl Environ Microbiol 2011, 77:8791-8794.
  • [37]Newton GJ, Mori S, Nakamura R, Hashimoto K, Watanabe K: Analyses of current-generating mechanisms of Shewanella loihica PV-4 and Shewanella oneidensis MR-1 in microbial fuel cells. Appl Environ Microbiol 2009, 75:7674-7681.
  • [38]Yong YC, Cai Z, Yu YY, Chen P, Jiang R, Cao B, Sun JZ, Wang JY, Song H: Increase of riboflavin biosynthesis underlies enhancement of extracellular electron transfer of Shewanella in alkaline microbial fuel cells. Bioresour Technol 2013, 130:763-768.
  • [39]Baron D, LaBelle E, Coursolle D, Gralnick JA, Bond DR: Electrochemical measurement of electron transfer kinetics by Shewanella oneidensis MR-1. J Biol Chem 2009, 284:28865-28873.
  • [40]Wu D, Xing D, Lu L, Wei M, Liu B, Ren N: Ferric iron enhances electricity generation by Shewanella oneidensis MR-1 in MFCs. Bioresour Technol 2013, 135:630-634.
  • [41]Park DH, Kim SK, Shin IH, Jeong YJ: Electricity production in biofuel cell using modified graphite electrode with Neutral Red. Biotechnol Lett 2000, 22:1301-1304.
  • [42]Mao L, Verwoerd WS: Genome-scale stoichiometry analysis to elucidate the innate capability of the cyanobacterium Synechocystis for electricity generation. J Ind Microbiol Biotechnol 2013, 40:1161-1180.
  • [43]Famili I, Förster J, Nielsen J, Palsson BO: Saccharomyces cerevisiae phenotypes can be predicted by using constraint-based analysis of a genome-scale reconstructed metabolic network. Proc Natl Acad Sci 2003, 100:13134-13139.
  • [44]Edwards JS, Ibarra RU, Palsson BO: In silico predictions of Escherichia coli metabolic capabilities are consistent with experimental data. Nat Biotechnol 2001, 19:125-130.
  • [45]Fong SS, Palsson BO: Metabolic gene-deletion strains of Escherichia coli evolve to computationally predicted growth phenotypes. Nat Genet 2004, 36:1056-1058.
  • [46]Varma A, Palsson BO: Stoichiometric flux balance models quantitatively predict growth and metabolic by-product secretion in wild-type Escherichia coli W3110. Appl Environ Microbiol 1994, 60:3724-3731.
  • [47]Ibarra RU, Edwards JS, Palsson BO: Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth. Nature 2002, 420:186-189.
  • [48]Burgard AP, Maranas CD: Optimization-based framework for inferring and testing hypothesized metabolic objective functions. Biotechnol Bioeng 2003, 82:670-677.
  • [49]Pereyra V, Saunders M, Castillo J: Equispaced Pareto front construction for constrained bi-objective optimization. Math Comput Model 2013, 57:2122-2131.
  • [50]Ekins S, Honeycutt JD, Metz JT: Evolving molecules using multi-objective optimization: applying to ADME/Tox. Drug Discov Today 2010, 15:451-460.
  • [51]Mao L, Verwoerd WS: Exploration and comparison of inborn microbial capacity of aerobic and anaerobic metabolisms of Saccharomyces cerevisiae for current production. Bioengineered 2013, 4:332-342.
  • [52]Mao L, Verwoerd WS: Computational comparison of mediated current generation capacity ofChlamydomonas reinhardtiiin photosynthetic and respiratory growth modes.J Biosci Bioeng 2014, 18:. No. 5 (November issue, 2014).
  • [53]Habicht KS, Salling L, Thamdrup B, Canfield DE: Effect of low sulfate concentrations on lactate oxidation and isotope fractionation during sulfate reduction by Archaeoglobus fulgidus strain Z. Appl Environ Microbiol 2005, 71:3770-3777.
  • [54]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.
  • [55]Virdis B, Freguia S, Rozendal RA, Rabaey K, Yuan Z, Keller J: 4.18 - Microbial fuel cells. In Treatise on Water Science. Edited by Oxford PW. Elsevier, Amsterdam; 2011:641-665.
  • [56]Sober HA, Company CR: Handbook of Biochemistry: Selected Data for Molecular Biology. Chemical Rubber Co, Cleveland, Ohio; 1968.
  • [57]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.
  • [58]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.
  • [59]Tang YJ, Martin HG, Dehal PS, Deutschbauer A, Llora X, Meadows A, Arkin A, Keasling JD: Metabolic flux analysis of Shewanella spp. reveals evolutionary robustness in central carbon metabolism. Biotechnol Bioeng 2009, 102:1161-1169.
  • [60]Song H-S, Ramkrishna D, Pinchuk GE, Beliaev AS, Konopka AE, Fredrickson JK: Dynamic modeling of aerobic growth of Shewanella oneidensis. Predicting triauxic growth, flux distributions, and energy requirement for growth. Metab Eng 2013, 15:25-33.
  • [61]Liu Y, Gao W, Wang Y, Wu L, Liu X, Yan T, Alm E, Arkin A, Thompson DK, Fields MW, Zhou J: Transcriptome analysis of Shewanella oneidensis MR-1 in response to elevated salt conditions. J Bacteriol 2005, 187:2501-2507.
  • [62]Mao L, Verwoerd WS: ORCA: a COBRA toolbox extension for model-driven discovery and analysis. Bioinformatics 2014, 30:584-585.
  文献评价指标  
  下载次数:55次 浏览次数:10次