Abstract
Microbial catalysis of carbon dioxide (CO2) reduction to multi-carbon compounds at the cathode is a highly attractive application of microbial electrosynthesis (MES). The microbes reduce CO2 by either taking the electrons or reducing the equivalents produced at the cathode. While using gaseous CO2 as the carbon source, the biological reduction process depends on the dissolution and mass transfer of CO2 in the electrolyte. In order to deal with this issue, a gas diffusion electrode (GDE) was investigated by feeding CO2 through the GDE into the MES reactor for its reduction at the biocathode. A combination of the catalyst layer (porous activated carbon and Teflon binder) and the hydrophobic gas diffusion layer (GDL) creates a three-phase interface at the electrode. So, CO2 and reducing equivalents will be available to the biocatalyst on the cathode surface. An enriched inoculum consisting of acetogenic bacteria, prepared from an anaerobic sludge, was used as a biocatalyst. The cathode potential was maintained at −1.1 V vs Ag/AgCl to facilitate direct and/or hydrogen-mediated CO2 reduction. Bioelectrochemical CO2 reduction mainly produced acetate but also extended the products to ethanol and butyrate. Average acetate production rates of 32 and 61 mg/L/day, respectively, with 20 and 80 % CO2 gas mixture feed were achieved with 10 cm2 of GDE. The maximum acetate production rate remained 238 mg/L/day for 20 % CO2 gas mixture. In conclusion, a gas diffusion biocathode supported bioelectrochemical CO2 reduction with enhanced mass transfer rate at continuous supply of gaseous CO2.
Similar content being viewed by others
Abbreviations
- A/m2 :
-
Ampere per square meter
- Atm:
-
Atmosphere
- CEM:
-
Cation exchange membrane
- CL:
-
Catalyst layer
- DO:
-
Dissolved oxygen
- GDE:
-
Gas diffusion electrode
- GDL:
-
Gas diffusion layer
- MES:
-
Microbial electrosynthesis
- k La:
-
Gas–liquid mass transfer coefficient
- NaBES:
-
Sodium 2-bromoethanesulfonate
- PTFE:
-
Polytetrafluoroethylene
- PVDF:
-
Polyvinylidene difluoride
- rpm:
-
Revolution per minute
- SHE:
-
Standard hydrogen electrode
- OD:
-
Optical density
- VFA:
-
Volatile fatty acid
References
Agler MT, Wrenn BA, Zinder SH, Angenent LT (2011) Waste to bioproduct conversion with undefined mixed cultures: the carboxylate platform. Trends Biotechnol 29:70–78. doi:10.1016/j.tibtech.2010.11.006
Alvarez-Gallego Y, Dominguez-Benetton X, Pant D, Diels L, Vanbroekhoven K, Genné I, Vermeiren P (2012) Development of gas diffusion electrodes for cogeneration of chemicals and electricity. Electrochim Acta 82:415–426. doi:10.1016/j.electacta.2012.06.096
Bajracharya S, ter Heijne A, Dominguez X, Strik DPBTB, Vanbroekhoven K, Buisman CJN, Pant D, ter Heijne A, Benetton XD, Vanbroekhoven K, Buisman CJN, Strik DPBTB, Pant D (2015) CO2 reduction by mixed and pure cultures in microbial electrosynthesis using an assembly of graphite felt and stainless steel as a cathode. Bioresour Technol. doi:10.1016/j.biortech.2015.05.081
Blanchet EM, Duquenne F, Rafrafi Y, Etcheverry L, Erable B, Bergel A (2015) Importance of the hydrogen route in up-scaling electrosynthesis for microbial CO2 reduction. Energy Environ Sci 8:3731–3744. doi:10.1039/C5EE03088A
Cassman KG, Liska AJ (2007) Food and fuel for all: realistic or foolish? Biofuels, Bioproducts and Biorefining 1:18–23. doi:10.1002/bbb.3
CAST (2006) Convergence of agriculture and energy : implications for research and policy, CAST commentary, QTA2006-3. Ames, Iowa
Chu S (2009) Carbon capture and sequestration. Science 325:1599. doi:10.1126/science.1181637
Cussler EL (1997) Diffusion: mass transfer in fluid systems, 2nd edn. Cambridge University Press, New York
Doucha J, Straka F, Lívanský K (2005) Utilization of flue gas for cultivation of microalgae (Chlorella sp.) in an outdoor open thin-layer photobioreactor. J Appl Phycol 17:403–412. doi:10.1007/s10811-005-8701-7
Drake HL, Gößner AS, Daniel SL (2008) Old acetogens, new light. Ann N Y Acad Sci 1125:100. doi:10.1196/annals.1419.016
Fan Y, Hongqiang H, Liu H, Fan Y, Hu H, Liu H (2007) Sustainable power generation in microbial fuel cells using bicarbonate buffer and proton transfer mechanisms. Environ Sci Technol 41:8154–8158. doi:10.1021/es071739c
Fast AG, Papoutsakis ET (2012) Stoichiometric and energetic analyses of non-photosynthetic CO2-fixation pathways to support synthetic biology strategies for production of fuels and chemicals. Curr Opin Chem Eng 1:380–395. doi:10.1016/j.coche.2012.07.005
Fernández, F.G.A., Grima, E.M., Sevilla, J.M.F., López, C.V.G., Moya, B.L., Aparicio, J.C.B., 2011. Liquid-phase gas collection. US2011015957 A1.
Fornero JJ, Rosenbaum M, Cotta MA, Angenent LT (2010) Carbon dioxide addition to microbial fuel cell cathodes maintains sustainable catholyte pH and improves anolyte pH, alkalinity, and conductivity. Environ Sci Technol 44:2728–2734. doi:10.1021/es9031985
Gabriel Acien Fernandez F, Gonzalez-Lopez CV, Fernandez Sevilla JM, Molina Grima E (2012) Conversion of CO2 into biomass by microalgae: how realistic a contribution may it be to significant CO2 removal? Appl Microbiol Biotechnol 96:577–586. doi:10.1007/s00253-012-4362-z
Ganigué R, Puig S, Batlle-Vilanova P, Balaguer MD, Colprim J (2015) Microbial electrosynthesis of butyrate from carbon dioxide. Chem Commun 51:3235–3238. doi:10.1039/C4CC10121A
González-López CV, Acién Fernández FG, Fernández-Sevilla JM, Sánchez Fernández JF, Molina Grima E (2012) Development of a process for efficient use of CO2 from flue gases in the production of photosynthetic microorganisms. Biotechnol Bioeng 109:1637–1650. doi:10.1002/bit.24446
HaoYu E, Cheng S, Scott K, Logan B (2007) Microbial fuel cell performance with non-Pt cathode catalysts. J Power Sources 171:275–281. doi:10.1016/j.jpowsour.2007.07.010
Hill GA (2006) Measurement of overall volumetric mass transfer coefficients for carbon dioxide in a well-mixed reactor using a pH probe. Ind Eng Chem Res 45:5796–5800. doi:10.1021/ie060242t
Hu P, Rismani-yazdi H, Gregory S (2013) Anaerobic CO2 fixation by the acetogenic bacterium Moorella thermoacetica. AICHE J 59:3176–3183. doi:10.1002/aic.14127
IPCC, 2014. Climate change 2014: synthesis report, Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland.
Jourdin L, Freguia S, Donose BC, Chen J, Wallace GG, Keller J, Flexer V (2014) A novel carbon nanotube modified scaffold as an efficient biocathode material for improved microbial electrosynthesis. J Mater Chem A 2:13093–13102. doi:10.1039/C4TA03101F
Jourdin L, Lu Y, Flexer V, Keller J, Freguia S (2015) Biologically-induced hydrogen production drives high rate/high efficiency microbial electrosynthesis of acetate from carbon dioxide. ChemElectroChem. doi:10.1002/celc.201500530
Kopljar D, Inan A, Vindayer P, Wagner N, Klemm E (2014) Electrochemical reduction of CO2 to formate at high current density using gas diffusion electrodes. J Appl Electrochem 44:1107–1116. doi:10.1007/s10800-014-0731-x
LaBelle EV, Marshall CW, Gilbert JA, May HD (2014) Influence of acidic pH on hydrogen and acetate production by an electrosynthetic microbiome. PLoS One 9:e109935
Le Quéré C, Peters GP, Andres RJ, Andrew RM, Boden TA, Ciais P, Friedlingstein P, Houghton RA, Marland G, Moriarty R, Sitch S, Tans P, Arneth A, Arvanitis A, Bakker DCE, Bopp L, Canadell JG, Chini LP, Doney SC, Harper A, Harris I, House JI, Jain AK, Jones SD, Kato E, Keeling RF, Klein Goldewijk K, Körtzinger A, Koven C, Lefèvre N, Maignan F, Omar A, Ono T, Park G-H, Pfeil B, Poulter B, Raupach MR, Regnier P, Rödenbeck C, Saito S, Schwinger J, Segschneider J, Stocker BD, Takahashi T, Tilbrook B, van Heuven S, Viovy N, Wanninkhof R, Wiltshire A, Zaehle S (2014) Global carbon budget 2013. Earth Syst Sci Data 6:235–263. doi:10.5194/essd-6-235-2014
Lee J, Little B (2015) Electrochemical and chemical complications resulting from yeast extract addition to stimulate microbial growth. Corrosion. doi:10.5006/1833
Lovley DR, Nevin KP (2013) Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr Opin Biotechnol 1–6. doi:10.1016/j.copbio.2013.02.012
Mahmood MN, Masheder D, Harty CJ (1987) Use of gas-diffusion electrodes for high-rate electrochemical reduction of carbon dioxide. I. Reduction at lead, indium- and tin-impregnated electrodes. J Appl Electrochem 17:1159–1170. doi:10.1007/BF01023599
Marshall CW, Ross DE, Fichot EB, Norman RS, May HD (2012) Electrosynthesis of commodity chemicals by an autotrophic microbial community. Appl Environ Microbiol 78:8412–8420. doi:10.1128/AEM.02401-12
Marshall CW, Ross DE, Fichot EB, Norman RS, May HD (2013) Long-term operation of microbial electrosynthesis systems improves acetate production by autotrophic microbiomes. Environ Sci Technol 47:6023–6029. doi:10.1021/es400341b
Modestra JA, Navaneeth B, Venkata Mohan S (2015) Bio-electrocatalytic reduction of CO2: enrichment of homoacetogens and pH optimization towards enhancement of carboxylic acids biosynthesis. J CO2 Util 10:78–87. doi:10.1016/j.jcou.2015.04.001
Mohanakrishna G, Seelam JS, Vanbroekhoven K, Pant D (2015) An enriched electroactive homoacetogenic biocathode for the microbial electrosynthesis of acetate through carbon dioxide reduction. Faraday Discuss. doi:10.1039/C5FD00041F
Naik SN, Goud VV, Rout PK, Dalai AK (2010) Production of first and second generation biofuels: a comprehensive review. Renew Sust Energ Rev 14:578–597
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 77:2882–2886. doi:10.1128/AEM.02642-10
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. MBio 1:e00103–e00110. doi:10.1128/mBio.00103-10.Editor
Oh S-E, Van Ginkel S, Logan BE (2003) The relative effectiveness of pH control and heat treatment for enhancing biohydrogen gas production. Environ Sci Technol 37:5186–5190. doi:10.1021/Es034291y
Pant D, Van Bogaert G, De Smet M, Diels L, Vanbroekhoven K (2010) Use of novel permeable membrane and air cathodes in acetate microbial fuel cells. Electrochim Acta 55:7710–7716. doi:10.1016/j.electacta.2009.11.086
Pasupuleti SB, Srikanth S, Venkata Mohan S, Pant D (2015) Continuous mode operation of microbial fuel cell (MFC) stack with dual gas diffusion cathode design for the treatment of dark fermentation effluent. Int J Hydrogen Energy 40:12424–12435. doi:10.1016/j.ijhydene.2015.07.049
Patil SA, Arends JBA, Vanwonterghem I, van Meerbergen J, Guo K, Tyson GW, Rabaey K (2015a) Selective enrichment establishes a stable performing community for microbial electrosynthesis of acetate from CO2. Environ Sci Technol 49(14):8833–8843
Patil SA, Gildemyn S, Pant D, Zengler K, Logan BE, Rabaey K (2015b) A logical data representation framework for electricity-driven bioproduction processes. Biotechnol Adv 33:736–744. doi:10.1016/j.biotechadv.2015.03.002
Rabaey K, Rozendal RA (2010) Microbial electrosynthesis—revisiting the electrical route for microbial production. Nat Rev Microbiol 8:706–716. doi:10.1038/nrmicro2422
Sakai S, Nakashimada Y, Yoshimoto H, Watanabe S, Okada H, Nishio N (2004) Ethanol production from H2 and CO2 by a newly isolated thermophilic bacterium, Moorella sp. HUC22-1. Biotechnol Lett 26:1607–1612. doi:10.1023/B:BILE.0000045661.03366.f2
Stams AJM, Plugge CM, De Bok FAM, Van Houten BHGW, Lens P, Dijkman H, Weijma J (2005) Metabolic interactions in methanogenic and sulfate-reducing bioreactors. Water Sci Technol 52:13–20
Steinbusch KJJ, Hamelers HVM, Schaap JD, Kampman C, Buisman CJN (2010) Bioelectrochemical ethanol production through mediated acetate reduction by mixed cultures. Environ Sci Technol 44:513–517. doi:10.1021/es902371e
Su M, Jiang Y, Li D (2013) Production of acetate from carbon dioxide in bioelectrochemical systems based on autotrophic mixed culture. J Microbiol Biotechnol 23:1140–1146
Talbot P, Gortares MP, Lencki RW, de la Noüe J (1991) Absorption of CO2 in algal mass culture systems: a different characterization approach. Biotechnol Bioeng 37:834–842. doi:10.1002/bit.260370907
Tracy BP, Jones SW, Fast AG, Indurthi DC, Papoutsakis ET (2012) Clostridia: the importance of their exceptional substrate and metabolite diversity for biofuel and biorefinery applications. Curr Opin Biotechnol 23:364–381. doi:10.1016/j.copbio.2011.10.008
Treybal RE (1981) Mass-transfer operations, 3 edn. McGraw-Hill, Inc
Vega JL, Prieto S, Elmore BB, Clausen EC, Gaddy JL (1989) The biological production of ethanol from synthesis gas. Appl Biochem Biotechnol 20-21:781–797. doi:10.1007/BF02936525
Whipple DT, Finke EC, Kenis PJA (2010) Microfluidic reactor for the electrochemical reduction of carbon dioxide: the effect of pH. Electrochem Solid-State Lett 13:B109. doi:10.1149/1.3456590
Ying K, Al-mashhadani MKH, Hanotu JO, Gilmour DJ, Zimmerman WB (2013) Enhanced mass transfer in microbubble driven airlift bioreactor for microalgal culture. Engineering 2013:735–743. doi:10.4236/eng.2013.59088
Zhang F, Cheng S, Pant D, Bogaert GV, Logan BE (2009) Power generation using an activated carbon and metal mesh cathode in a microbial fuel cell. Electrochem Commun 11:2177–2179. doi:10.1016/j.elecom.2009.09.024
Zhang K, Miyachi S, Kurano N (2001) Photosynthetic performance of a cyanobacterium in a vertical flat-plate photobioreactor for outdoor microalgal production and fixation of CO2. Biotechnol Lett 23:21–26. doi:10.1023/A:1026737000160
Zhang X, Pant D, Zhang F, Liu J, He W, Logan BE (2014) Long-term performance of chemically and physically modified activated carbons in air cathodes of microbial fuel cells. ChemElectroChem 1:1859–1866. doi:10.1002/celc.201402123
Acknowledgments
The work was supported by a PhD grant to Suman Bajracharya from VITO’s strategic research funds. The authors acknowledge Mr. Shishir Kanti Pramanik for conducting the gas transfer experiments and taking samples from the reactor.
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Philippe Garrigues
Highlights
• The first application of gas diffusion electrode (GDE) as a biocathode in MES supported CO2 reduction to multi-carbon compounds.
• A mixed culture predominantly exhibiting the homoacetogenic activity catalyzed the bioelectrochemical CO2 reduction.
• Methanogenic activity was successfully suppressed from the mixed culture originating from wastewater sludge after a heat treatment and series of sub-culturing to enrich acetogenic activity.
• The use of GDE enhanced the mass transfer of gaseous substrates compared to the supply through conventional spargers in submerged electrode.
• Bioelectrochemical CO2 reduction with a gas diffusion biocathode produced acetate as the main product and ethanol and butyrate as secondary products.
Electronic supplementary material
ESM. 1
(DOCX 94 kb)
Rights and permissions
About this article
Cite this article
Bajracharya, S., Vanbroekhoven, K., Buisman, C.J. et al. Application of gas diffusion biocathode in microbial electrosynthesis from carbon dioxide. Environ Sci Pollut Res 23, 22292–22308 (2016). https://doi.org/10.1007/s11356-016-7196-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-016-7196-x