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Microbial Electrosynthesis I: Pure and Defined Mixed Culture Engineering

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Bioelectrosynthesis

Part of the book series: Advances in Biochemical Engineering/Biotechnology ((ABE,volume 167))

Abstract

In the past 6 years, microbial bioelectrochemistry has strongly increased in attraction and audience when expanding from mainly environmental technology applications to biotechnology. In particular, the promise to combine electrosynthesis with microbial catalysis opens attractive approaches for new sustainable redox-cofactor recycling, redox-balancing, or even biosynthesis processes. Much of this promise is still not fulfilled, but it has opened and fueled entirely new research areas in this discipline. Activities in designing, tailoring, and applying specific microbial catalysts as pure or defined co-cultures for defined target bioproductions are greatly accelerating. This chapter gives an overview of the current progress as well as the emerging trends in molecular and ecological engineering of defined microbial biocatalysts to prepare them for evolving microbial electrosynthesis processes. In addition, the multitude of microbial electrosynthetic processes with complex undefined mixed cultures is covered by ter Heijne et al. (Adv Biochem Eng Biotechnol. https://doi.org/10.1007/10_2017_15, 2017).

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References

  1. Nevin KP, Woodard TL, Franks AE, Summers ZM, Lovley DR (2010) Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. MBio 1(2):e00103–e00110

    Google Scholar 

  2. Simonte F et al (2017) Extracellular electron transfer and biosensors. Adv Biochem Eng Biotechnol. https://doi.org/10.1007/10_2017_34

    Google Scholar 

  3. Nevin KP, Hensley SA, Franks AE, Summers ZM, Ou J, Woodard TL, Snoeyenbos-West OL, Lovley DR (2011) Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microbiol 77(9):2882–2886

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Rosenbaum MA, Henrich AW (2014) Engineering microbial electrocatalysis for chemical and fuel production. Curr Opin Biotechnol 29:93–98

    CAS  PubMed  Google Scholar 

  5. ter Heijne A et al (2017) Mixed culture biocathodes for production of hydrogen, methane and carboxylates. Adv Biochem Eng Biotechnol. https://doi.org/10.1007/10_2017_15

    Google Scholar 

  6. Flynn JM, Ross DE, Hunt KA, Bond DR, Gralnick JA (2010) Enabling unbalanced fermentations by using engineered electrode-interfaced bacteria. mBio 1(5):e00190–10

    PubMed  PubMed Central  Google Scholar 

  7. Gescher JS, Cordova CD, Spormann AM (2008) Dissimilatory iron reduction in Escherichia coli: identification of CymA of Shewanella oneidensis and NapC of E. coli as ferric reductases. Mol Microbiol 68(3):706–719

    CAS  PubMed  Google Scholar 

  8. Goldbeck CP, Jensen HM, TerAvest MA, Beedle N, Appling Y, Hepler M, Cambray G, Mutalik V, Angenent LT, Ajo-Franklin CM (2013) Tuning promoter strengths for improved synthesis and function of electron conduits in Escherichia coli. ACS Synth Biol 2(3):150–159

    CAS  PubMed  Google Scholar 

  9. Jensen HM, Albers AE, Malley KR, Londer YY, Cohen BE, Helms BA, Weigele P, Groves JT, Ajo-Franklin CM (2010) Engineering of a synthetic electron conduit in living cells. Proc Natl Acad Sci U S A 107(45):19213–19218

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Pitts KE, Dobbin PS, Reyes-Ramirez F, Thomson AJ, Richardson DJ, Seward HE (2003) Characterization of the Shewanella oneidensis MR-1 decaheme cytochrome MtrA: expression in Escherichia coli confers the ability to reduce soluble Fe(III) chelates. J Biol Chem 278(30):27758–27765

    CAS  PubMed  Google Scholar 

  11. Schuetz B, Schicklberger M, Kuermann J, Spormann AM, Gescher J (2009) Periplasmic electron transfer via the c-type cytochromes MtrA and FccA of Shewanella oneidensis MR-1. Appl Environ Microbiol 75(24):7789–7796

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Sturm-Richter K, Golitsch F, Sturm G, Kipf E, Dittrich A, Beblawy S, Kerzenmacher S, Gescher J (2015) Unbalanced fermentation of glycerol in Escherichia coli via heterologous production of an electron transport chain and electrode interaction in microbial electrochemical cells. Bioresour Technol 186:89–96

    CAS  PubMed  Google Scholar 

  13. TerAvest MA, Zajdel TJ, Ajo-Franklin CM (2014) The Mtr pathway of Shewanella oneidensis MR-1 couples substrate utilization to current production in Escherichia coli. ChemElectroChem 1(11):1874–1879

    CAS  Google Scholar 

  14. Loeschcke A, Thies S (2015) Pseudomonas putida-a versatile host for the production of natural products. Appl Microbiol Biotechnol 99(15):6197–6214

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Hintermayer S, Yu S, Krömer JO, Weuster-Botz D (2016) Anodic respiration of Pseudomonas putida KT2440 in a stirred-tank bioreactor. Biochem Eng J 115:1–13

    CAS  Google Scholar 

  16. Lai B, Yu S, Bernhardt PV, Rabaey K, Virdis B, Krömer JO (2016) Anoxic metabolism and biochemical production in Pseudomonas putida F1 driven by a bioelectrochemical system. Biotechnol Biofuels 9:39

    PubMed  PubMed Central  Google Scholar 

  17. Schmitz S, Nies S, Wierckx N, Blank LM, Rosenbaum MA (2015) Engineering mediator-based electroactivity in the obligate aerobic bacterium Pseudomonas putida KT2440. Front Microbiol 6:284

    PubMed  PubMed Central  Google Scholar 

  18. Venkataraman A, Rosenbaum M, Arends JBA, Halitsche R, Angenent LT (2010) Quorum sensing regulates electric current generation of Pseudomonas aeruginosa PA14 in bioelectrochemical systems. Electrochem Commun 12(3):459–462

    CAS  Google Scholar 

  19. Lohner ST, Deutzmann JS, Logan BE, Leigh J, Spormann AM (2014) Hydrogenase-independent uptake and metabolism of electrons by the archaeon Methanococcus maripaludis. ISME J 8(8):1673–1681

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Ammam F, Tremblay PL, Lizak DM, Zhang T (2016) Effect of tungstate on acetate and ethanol production by the electrosynthetic bacterium Sporomusa ovata. Biotechnol Biofuels 9:163

    PubMed  PubMed Central  Google Scholar 

  21. Giddings CG, Nevin KP, Woodward T, Lovley DR, Butler CS (2015) Simplifying microbial electrosynthesis reactor design. Front Microbiol 6:468

    PubMed  PubMed Central  Google Scholar 

  22. Li H, Opgenorth PH, Wernick DG, Rogers S, TY W, Higashide W, Malati P, Huo YX, Cho KM, Liao JC (2012) Integrated electromicrobial conversion of CO2 to higher alcohols. Science 335:1596

    CAS  PubMed  Google Scholar 

  23. Grousseau E, Lu J, Gorret N, Guillouet SE, Sinskey AJ (2014) Isopropanol production with engineered Cupriavidus necator as bioproduction platform. Appl Microbiol Biotechnol 98:4277–4290

    CAS  PubMed  Google Scholar 

  24. Torella JP, Gagliardi CJ, Chen JS, Bediako DK, Colon B, Way JC, Silver PA, Nocera DG (2015) Efficient solar-to-fuels production from a hybrid microbial-water-splitting catalyst system. Proc Natl Acad Sci U S A 112(8):2337–2342

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Chandrayan SK, McTernan PM, Hopkins RC, Sun JS, Jenney FE, Adams MWW (2012) Engineering hyperthermophilic archaeon Pyrococcus furiosus to overproduce its cytoplasmic [NiFe]-hydrogenase. J Biol Chem 287(5):3257–3264

    CAS  PubMed  Google Scholar 

  26. Keller MW, Schut GJ, Lipscomb GL, Menon AL, Iwuchukwu IJ, Leuko TT, Thorgersen MP, Nixon WJ, Hawkins AS, Kelly RM, Adams MWW (2013) Exploiting microbial hyperthermophilicity to produce an industrial chemical, using hydrogen and carbon dioxide. Proc Natl Acad Sci U S A 110(15):5840–5845

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 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 (2006) Electrically conductive bacterial nanowires produced by Shewanella oneidensis strain MR-1 and other microorganisms. Proc Natl Acad Sci U S A 103(30):11358–11363

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Gregory KB, Bond DR, Lovley DR (2004) Graphite electrodes as electron donors for anaerobic respiration. Environ Microbiol 6(6):596–604

    CAS  PubMed  Google Scholar 

  29. Deutzmann JS, Sahin M, Spormann AM (2015) Extracellular enzymes facilitate electron uptake in biocorrosion and bioelectrosynthesis. mBio 6(2):e00496–15

    PubMed  PubMed Central  Google Scholar 

  30. Höffner K, Barton PI (2014) Design of microbial consortia for industrial biotechnology. Comput Aided Chem Eng 34:65–74

    Google Scholar 

  31. Bernstein HC, Carlson RP (2012) Microbial consortia engineering for cellular factories: in vitro to in silico systems. Comput Struct Biotechnol J 3(4):1–8

    Google Scholar 

  32. Yang Y, Wu Y, Hu Y, Cao Y, Poh CL, Cao B, Song H (2015) Engineering electrode-attached microbial consortia for high-performance xylose-fed microbial fuel cell. ACS Catal 5(11):6937–6945

    CAS  Google Scholar 

  33. Song H, Ding M-Z, Jia X-Q, Ma Q, Yuan Y-J (2014) Synthetic microbial consortia: from systematic analysis to construction and applications. Chem Soc Rev 43(20):6954–6981

    CAS  PubMed  Google Scholar 

  34. Deutzmann JS, Spormann AM (2017) Enhanced microbial electrosynthesis by using defined co-cultures. ISME J 11(3):704–714

    CAS  PubMed  Google Scholar 

  35. Tao L, Wang H, Xie M, Thia L, Chen WN, Wang X (2015) Improving mediated electron transport in anodic bioelectrocatalysis. Chem Commun 51(61):12170–12173

    CAS  Google Scholar 

  36. Marsili E, Baron DB, Shikhare ID, Coursolle D, Gralnick JA, Bond DR (2008) Shewanella secretes flavins that mediate extracellular electron transfer. Proc Natl Acad Sci U S A 105(10):3968–3973

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Tokunou Y, Hashimoto K, Okamoto A (2016) Acceleration of extracellular electron transfer by alternative redox-active molecules to riboflavin for outer-membrane cytochrome c of Shewanella oneidensis MR-1. J Phys Chem C 120(29):16168–16173

    CAS  Google Scholar 

  38. Liu T, YY Y, Chen T, Chen WN (2016) A synthetic microbial consortium of Shewanella and Bacillus for enhanced generation of bioelectricity. Biotechnol Bioeng 114(3):526–532

    PubMed  Google Scholar 

  39. Rodionov DA, Yang C, Li X, Rodionova IA, Wang Y, Obraztsova AY, Zagnitko OP, Overbeek R, Romine MF, Reed S (2010) Genomic encyclopedia of sugar utilization pathways in the Shewanella genus. BMC Genomics 11(1):1

    Google Scholar 

  40. Kim C, Song YE, Lee CR, Jeon B-H, Kim JR (2016) Glycerol-fed microbial fuel cell with a co-culture of Shewanella oneidensis MR-1 and Klebsiella pneumonae J2B. J Ind Microbiol Biotechnol 43(10):1397–1403

    CAS  PubMed  Google Scholar 

  41. Rosenbaum M, Aulenta F, Villano M, Angenent LT (2011) Cathodes as electron donors for microbial metabolism: which extracellular electron transfer mechanisms are involved? Bioresour Technol 102(1):324–333

    CAS  PubMed  Google Scholar 

  42. Wang VB, Chua S-L, Cai Z, Sivakumar K, Zhang Q, Kjelleberg S, Cao B, Loo SCJ, Yang L (2014) A stable synergistic microbial consortium for simultaneous azo dye removal and bioelectricity generation. Bioresour Technol 155:71–76

    CAS  PubMed  Google Scholar 

  43. Caccavo F, Lonergan DJ, Lovley DR, Davis M, Stolz JF, Mcinerney MJ (1994) Geobacter sulfurreducens sp-nov, a hydrogen-oxidizing and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol 60(10):3752–3759

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Qu Y, Feng Y, Wang X, Logan BE (2012) Use of a coculture to enable current production by Geobacter sulfurreducens. Appl Environ Microbiol 78(9):3484–3487

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Speers AM, Young JM, Reguera G (2014) Fermentation of glycerol into ethanol in a microbial electrolysis cell driven by a customized consortium. Environ Sci Technol 48(11):6350–6358

    CAS  PubMed  Google Scholar 

  46. Speers AM, Reguera G (2012) Consolidated bioprocessing of AFEX-pretreated corn stover to ethanol and hydrogen in a microbial electrolysis cell. Environ Sci Technol 46(14):7875–7881

    CAS  PubMed  Google Scholar 

  47. Ren Z, Ward TE, Regan JM (2007) Electricity production from cellulose in a microbial fuel cell using a defined binary culture. Environ Sci Technol 41(13):4781–4786

    CAS  PubMed  Google Scholar 

  48. Venkataraman A, Rosenbaum MA, Perkins SD, Werner JJ, Angenent LT (2011) Metabolite-based mutualism between Pseudomonas aeruginosa PA14 and Enterobacter aerogenes enhances current generation in bioelectrochemical systems. Energy Environ Sci 4(11):4550

    CAS  Google Scholar 

  49. Read ST, Dutta P, Bond PL, Keller J, Rabaey K (2010) Initial development and structure of biofilms on microbial fuel cell anodes. BMC Microbiol 10(1):1

    Google Scholar 

  50. Harnisch F, Rosa LF, Kracke F, Virdis B, Krömer JO (2015) Electrifying white biotechnology: engineering and economic potential of electricity-driven bio-production. ChemSusChem 8(5):758–766

    CAS  PubMed  Google Scholar 

  51. Escapa A, Mateos R, Martínez E, Blanes J (2016) Microbial electrolysis cells: an emerging technology for wastewater treatment and energy recovery. From laboratory to pilot plant and beyond. Renew Sust Energ Rev 55:942–956

    CAS  Google Scholar 

  52. Moscoviz R, Toledo-Alarcón J, Trably E, Bernet N (2016) Electro-fermentation: how to drive fermentation using electrochemical systems. Trends Biotechnol 34(11):856–865

    CAS  PubMed  Google Scholar 

  53. Tremblay P-L, Zhang T (2015) Electrifying microbes for the production of chemicals. Front Microbiol 6:201

    PubMed  PubMed Central  Google Scholar 

  54. Kiely PD, Regan JM, Logan BE (2011) The electric picnic: synergistic requirements for exoelectrogenic microbial communities. Curr Opin Biotechnol 22(3):378–385

    CAS  PubMed  Google Scholar 

  55. Shong J, Diaz MRJ, Collins CH (2012) Towards synthetic microbial consortia for bioprocessing. Curr Opin Biotechnol 23(5):798–802

    CAS  PubMed  Google Scholar 

  56. Miceli JF, Garcia-Peña I, Parameswaran P, Torres CI, Krajmalnik-Brown R (2014) Combining microbial cultures for efficient production of electricity from butyrate in a microbial electrochemical cell. Bioresour Technol 169:169–174

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Sun D, Call DF, Kiely PD, Wang A, Logan BE (2012) Syntrophic interactions improve power production in formic acid fed MFCs operated with set anode potentials or fixed resistances. Biotechnol Bioeng 109(2):405–414

    CAS  PubMed  Google Scholar 

  58. Torres CI, Krajmalnik-Brown R, Parameswaran P, Marcus AK, Wanger G, Gorby YA, Rittmann BE (2009) Selecting anode-respiring bacteria based on anode potential: phylogenetic, electrochemical, and microscopic characterization. Environ Sci Technol 43(24):9519–9524

    CAS  PubMed  Google Scholar 

  59. Kadier A, Simayi Y, Abdeshahian P, Azman NF, Chandrasekhar K, Kalil MS (2016) A comprehensive review of microbial electrolysis cells (MEC) reactor designs and configurations for sustainable hydrogen gas production. Alex Eng J 55(1):427–443

    Google Scholar 

  60. Baudler A, Schmidt I, Langner M, Greiner A, Schröder U (2015) Does it have to be carbon? Metal anodes in microbial fuel cells and related bioelectrochemical systems. Energy Environ Sci 8(7):2048–2055

    CAS  Google Scholar 

  61. Gimkiewicz C, Hunger S, Harnisch F (2016) Evaluating the feasibility of microbial electrosynthesis based on Gluconobacter oxydans. ChemElectroChem 3(9):1337–1346

    CAS  Google Scholar 

  62. Minty JJ, Singer ME, Scholz SA, Bae CH, Ahn JH, Foster CE, Liao JC, Lin XN (2013) Design and characterization of synthetic fungal-bacterial consortia for direct production of isobutanol from cellulosic biomass. Proc Natl Acad Sci U S A 110(36):14592–14597

    CAS  PubMed  PubMed Central  Google Scholar 

  63. Schievano A, Sciarria TP, Vanbroekhoven K, De Wever H, Puig S, Andersen SJ, Rabaey K, Pant D (2016) Electro-fermentation–merging electrochemistry with fermentation in industrial applications. Trends Biotechnol 34(11):866–878

    CAS  PubMed  Google Scholar 

  64. Goers L, Freemont P, Polizzi KM (2014) Co-culture systems and technologies: taking synthetic biology to the next level. J R Soc Interface 11(96):20140065

    PubMed  PubMed Central  Google Scholar 

  65. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31(3):233–239

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Kracke F, Krömer JO (2014) Identifying target processes for microbial electrosynthesis by elementary mode analysis. BMC Bioinf 15:410

    Google Scholar 

  67. Choi O, Kim T, Woo HM, Um Y (2014) Electricity-driven metabolic shift through direct electron uptake by electroactive heterotroph Clostridium pasteurianum. Sci Rep 4:6961

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Liew F, Martin ME, Tappel RC, Heijstra BD, Mihalcea C, Kopke M (2016) Gas fermentation-a flexible platform for commercial scale production of low-carbon-fuels and chemicals from waste and renewable feedstocks. Front Microbiol 7:694

    PubMed  PubMed Central  Google Scholar 

  69. Zengler K, Palsson BO (2012) A road map for the development of community systems (CoSy) biology. Nat Rev Microbiol 10(5):366–372

    CAS  PubMed  Google Scholar 

  70. Johns NI, Blazejewski T, Gomes AL, Wang HH (2016) Principles for designing synthetic microbial communities. Curr Opin Microbiol 31:146–153

    PubMed  PubMed Central  Google Scholar 

  71. Klitgord N, Segre D (2010) Environments that induce synthetic microbial ecosystems. PLoS Comput Biol 6(11):e1001002

    PubMed  PubMed Central  Google Scholar 

  72. Zampieri M, Sauer U (2016) Model-based media selection to minimize the cost of metabolic cooperation in microbial ecosystems. Bioinformatics 32(11):1733–1739

    CAS  PubMed  Google Scholar 

  73. Pandit AV, Mahadevan R (2011) In silico characterization of microbial electrosynthesis for metabolic engineering of biochemicals. Microb Cell Factories 10(1):1

    Google Scholar 

  74. Kouzuma A, Kato S, Watanabe K (2015) Microbial interspecies interactions: recent findings in syntrophic consortia. Front Microbiol 6:477

    PubMed  PubMed Central  Google Scholar 

  75. Shrestha PM, Rotaru AE (2014) Plugging in or going wireless: strategies for interspecies electron transfer. Front Microbiol 5:237

    PubMed  PubMed Central  Google Scholar 

  76. Kobayashi H, Saito N, Fu Q, Kawaguchi H, Vilcaez J, Wakayama T, Maeda H, Sato K (2013) Bio-electrochemical property and phylogenetic diversity of microbial communities associated with bioelectrodes of an electromethanogenic reactor. J Biosci Bioeng 116(1):114–117

    CAS  PubMed  Google Scholar 

  77. Rotaru A-E, Shrestha PM, Liu F, Ueki T, Nevin K, Summers ZM, Lovley DR (2012) Interspecies electron transfer via hydrogen and formate rather than direct electrical connections in cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens. Appl Environ Microbiol 78(21):7645–7651

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Summers ZM, Fogarty HE, Leang C, Franks AE, Malvankar NS, Lovley DR (2010) Direct exchange of electrons within aggregates of an evolved syntrophic coculture of anaerobic bacteria. Science 330(6009):1413–1415

    CAS  PubMed  Google Scholar 

  79. Chuang JS, Rivoire O, Leibler S (2010) Cooperation and Hamilton's rule in a simple synthetic microbial system. Mol Syst Biol 6(1):398

    PubMed  PubMed Central  Google Scholar 

  80. Wintermute EH, Silver PA (2010) Emergent cooperation in microbial metabolism. Mol Syst Biol 6(1):407

    PubMed  PubMed Central  Google Scholar 

  81. Clinton A, Rumbaugh KP (2015) Interspecies and interkingdom signaling via Quorum signals. Isr J Chem 56(5):265–272

    Google Scholar 

  82. Rabaey K, Rozendal RA (2010) Microbial electrosynthesis — revisiting the electrical route for microbial production. Nat Rev Microbiol 8(10):706–716

    CAS  PubMed  Google Scholar 

  83. Diender M, Stams AJ, Sousa DZ (2016) Production of medium-chain fatty acids and higher alcohols by a synthetic co-culture grown on carbon monoxide or syngas. Biotechnol Biofuels 9(1):1

    Google Scholar 

  84. Xiao Z, Awata T, Zhang D, Katayama A (2016) Denitrification by Pseudomonas stutzeri coupled with CO2 reduction by Sporomusa ovata with hydrogen as an electron donor assisted by solid-phase humin. J Biosci Bioeng 122(3):307–313

    CAS  PubMed  Google Scholar 

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Correspondence to Miriam A. Rosenbaum .

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Rosenbaum, M.A., Berger, C., Schmitz, S., Uhlig, R. (2017). Microbial Electrosynthesis I: Pure and Defined Mixed Culture Engineering. In: Harnisch, F., Holtmann, D. (eds) Bioelectrosynthesis. Advances in Biochemical Engineering/Biotechnology, vol 167. Springer, Cham. https://doi.org/10.1007/10_2017_17

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