Microbial electrosynthesis of organic chemicals from CO₂ by Clostridium scatologenes ATCC 25775^T

Abstract

Background

The conversion of CO₂ into high value-added products has a very important environmental and economic significance. Microbial electrosynthesis (MES) is a promising technology, which adopts a bioelectrochemical system to transform CO₂ into organic chemicals.

Results

In this study, Clostridium scatologenes ATCC 25775^T, an anaerobic acetogenic bacterium, demonstrated its utility as a biocatalyst in a MES system, for the first time. With the cathodic potential of the MES system decreased from − 0.6 to − 1.2 V (vs. Ag/AgCl), the current density of the MES, and the production of organic chemicals, increased. Combining the genetic analysis and the results of the wet lab experiments, we believe C. scatologenes may accept electrons directly from the cathode to reduce CO₂ into organic compounds at a potential of − 0.6 V. The acetic and butyric acid reached a maximum value of 0.03 and 0.01 g/L, respectively, and the maximum value of total coulombic efficiency was about 84%, at the potential of − 0.6 V. With the decrease in cathodic potentials, both direct electron transfer and exogenous electron shuttle, H₂ might be adopted for the C. scatologenes MES system. At a potential of − 1.2 V, acetic acid, butyric acid and ethanol were detected in the cathodic chamber, with their maximum values increasing to 0.44, 0.085 and 0.015 g/L, respectively. However, due to the low H₂ utilization rate by the C. scatologenes planktonic cell, the total coulombic efficiency of the MES system dropped to 37.8%.

Conclusion

Clostridium scatologenes is an acetogenic bacterium which may fix CO₂ through the Wood–Ljungdahl pathway. Under H₂ fermentation, C. scatologenes may reduce CO₂ to acetic acid, butyric acid and ethanol. It can also be used as the biocatalyst in MES systems.

Keywords

Clostridium scatologenes ATCC 25775^T / Microbial electrosynthesis / CO₂

References

[1] Bajracharya S, Srikanth S, Mohanakrishna G, Zacharia R, Strik DPBTB, Pant D. Biotransformation of carbon dioxide in bioelectrochemical systems: State of the art and future prospects. J Power Sources, 2017, 356: 256-273.

[2] Batlle-Vilanova P, Puig S, Gonzalez-Olmos R, Balaguer MD, Colprim J. Continuous acetate production through microbial electrosynthesis from CO₂ with microbial mixed culture. J Chem Technol Biotechnol, 2016, 91: 921-927.

[3] Batlle-Vilanova P, Ganigue R, Ramio-Pujol S, Baneras L, Jimenez G, Hidalgo M, Balaguer MD, Colprim J, Puig S. Microbial electrosynthesis of butyrate from carbon dioxide: production and extraction. Bioelectrochemistry, 2017, 117: 57-64.

[4] Cheng SA, Xing DF, Call DF, Logan BE. Direct biological conversion of electrical current into methane by electromethanogenesis. Environ Sci Technol, 2009, 43: 3953-3958.

[5] Chu T, Sai HT, Wu D, Wu JCS, Tzu H. Application of optical-fiber photoreactor for CO₂ photocatalytic reduction. Topics Catal, 2008, 47: 131-137.

[6] Faraghiparapari N, Zengler K. Production of organics from CO₂ by microbial electrosynthesis (MES) at high temperature. J Chem Technol Biotechnol, 2017, 92: 375-381.

[7] Giddings CGS, Nevin KP, Woodward T, Lovley DR, Butler CS. Simplifying microbial electrosynthesis reactor design. Front Microbiol, 2015, 6: 648.

[8] Gildemyn S, Verbeeck K, Slabbinck R, Andersen SJ, Prevoteau A, Rabaey K. Integrated production, extraction, and concentration of acetic acid from CO₂ through microbial electrosynthesis. Environ Sci Tech Lett, 2015, 2: 325-328.

[9] Gong YM, Ebrahim A, Feist AM, Embree M, Zhang T, Lovley D, Zengler K. Sulfide-driven microbial electrosynthesis. Environ Sci Technol, 2013, 47: 568-573.

[10] Holdeman LV, WEC Moore (1977) Anaerobe laboratory manual

[11] Huang L, Jiang L, Wang Q, Quan X, Yang J, Chen L. Cobalt recovery with simultaneous methane and acetate production in biocathode microbial electrolysis cells. Chem Eng J, 2014, 253: 281-290.

[12] Huber MT. Energizing historical materialism: fossil fuels, space and the capitalist mode of production. Geoforum, 2009, 40: 105-116.

[13] Jourdin L, Freguia S, Donose BC, Chen J, Wallace GG, Keller J, Flexer V. A novel carbon nanotube modified scaffold as an efficient biocathode material for improved microbial electrosynthesis. J Mater Chem A, 2014, 2: 13093-13102.

[14] Jourdin L, Grieger T, Monetti J, Flexer V, Freguia S, Lu Y, Chen J, Romano M, Wallace GG, Keller J. High acetic acid production rate obtained by microbial electrosynthesis from carbon dioxide. Environ Sci Technol, 2015, 49: 13566-13574.

[15] Karelovic A, Bargibant A, Fernandez C, Ruiz P. Effect of the structural and morphological properties of Cu/ZnO catalysts prepared by citrate method on their activity toward methanol synthesis from CO₂ and H₂ under mild reaction conditions. Catal Today, 2012, 197: 109-118.

[16] Kim TS, Kim BH. Electron flow shift in clostridium-acetobutylicum fermentation by electrochemically introduced reducing equivalent. Biotechnol Lett, 1988, 10: 123-128.

[17] Kim HY, Choi I, Ahn SH, Hwang SJ, Yoo SJ, Han J, Kim J, Park H, Jang JH, Kim SK. Analysis on the effect of operating conditions on electrochemical conversion of carbon dioxide to formic acid. Int J Hydrogen Energy, 2014, 39: 16506-16512.

[18] Kusel K, Dorsch T, Acker G, Stackebrandt E, Drake HL. Clostridium scatologenes strain SL1 isolated as an acetogenic bacterium from acidic sediments. Int J Syst Evol Microbiol, 2000, 50: 537-546.

[19] Liao JC, Mi L, Pontrelli S, Luo S. Fuelling the future: microbial engineering for the production of sustainable biofuels. Nat Rev Microbiol, 2016, 14: 288-304.

[20] Lovley DR. Live wires: direct extracellular electron exchange for bioenergy and the bioremediation of energy-related contamination. Energy Environ Sci, 2011, 4: 4896-4906.

[21] Lovley DR. Powering microbes with electricity: direct electron transfer from electrodes to microbes. Env Microbiol Rep, 2011, 3: 27-35.

[22] Lovley DR, Nevin KP. Electrobiocommodities: powering microbial production of fuels and commodity chemicals from carbon dioxide with electricity. Curr Opin Biotechnol, 2013, 24: 385-390.

[23] Marshall CW, Ross DE, Fichot EB, Norman RS, May HD. Long-term operation of microbial electrosynthesis systems improves acetate production by autotrophic microbiomes. Environ Sci Technol, 2013, 47: 6023-6029.

[24] Nevin KP, Woodard TL, Franks AE, Summers ZM, Lovley DR. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. Mbio, 2010, 1: e00103-e00110.

[25] Nevin KP, Hensley SA, Franks AE, Summers ZM, Ou JH, Woodard TL, Snoeyenbos-West OL, Lovley DR. Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microb, 2011, 77: 2882-2886.

[26] Nie HR, Zhang T, Cui MM, Lu HY, Lovley DR, Russell TP. Improved cathode for high efficient microbial-catalyzed reduction in microbial electrosynthesis cells. Phys Chem Chem Phys, 2013, 15: 14290-14294.

[27] Nowak DJ, Crane DE. Carbon storage and sequestration by urban trees in the USA. Environ Pollut, 2002, 116: 381-389.

[28] Olah GAP, SuryaViva GK, Federico A. Electrochemical reduction of CO₂ over Sn-Nafion® coated electrode for a fuel-cell-like device. J Power Sources, 2013, 223: 68-74.

[29] O’Neill BC, Oppenheimer M. Climate change—dangerous climate impacts and the Kyoto protocol. Science, 2002, 296: 1971-1972.

[30] Patil SA, Gildemyn S, Pant D, Zengler K, Logan BE, Rabaey K. A logical data representation framework for electricity-driven bioproduction processes. Biotechnol Adv, 2015, 33: 736-744.

[31] Pearson RJ, Eisaman MD, Turner JWG, Edwards PP, Jiang Z, Kuznetsov VL, Littau KA, Di Marco L, Taylor SRG. Energy storage via carbon-neutral fuels made from CO₂, water, and renewable energy. Proc IEEE, 2012, 100: 440-460.

[32] Rozendal RA, Leone E, Keller J, Rabaey K. Efficient hydrogen peroxide generation from organic matter in a bioelectrochemical system. Electrochem Commun, 2009, 11: 1752-1755.

[33] Schuchmann K, Muller V. Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria. Nat Rev Microbiol, 2014, 12: 809-821.

[34] Shin HJ, Jung KA, Nam CW, Park JM. A genetic approach for microbial electrosynthesis system as biocommodities production platform. Bioresour Technol, 2017, 245: 1421-1429.

[35] Si RW, Zhai DD, Liao ZH, Gao L, Yong YC. A whole-cell electrochemical biosensing system based on bacterial inward electron flow for fumarate quantification. Biosens Bioelectron, 2015, 68: 34-40.

[36] Smith LD. Common mesophilic anaerobes, including Clostridium botulinum and Clostridium tetani, in 21 soil specimens. Appl Microbiol, 1975, 29: 590-594.

[37] Song TS, Zhang H, Liu H, Zhang D, Wang H, Yang Y, Yuan H, Xie J. High efficiency microbial electrosynthesis of acetate from carbon dioxide by a self-assembled electroactive biofilm. Bioresour Technol, 2017, 243: 573-582.

[38] Steinbusch KJJ, Hamelers HVM, Schaap JD, Kampman C, Buisman CJN. Bioelectrochemical ethanol production through mediated acetate reduction by mixed cultures. Environ Sci Technol, 2010, 44: 513-517.

[39] Tremblay PL, Zhang T. Electrifying microbes for the production of chemicals. Front Microbiol, 2015, 6: 201.

[40] Yang Y, Yu YY, Wang YZ, Zhang CL, Wang JX, Fang Z, Lv H, Zhong JJ, Yong YC. Amplification of electrochemical signal by a whole-cell redox reactivation module for ultrasensitive detection of pyocyanin. Biosens Bioelectron, 2017, 98: 338-344.

[41] Yin Y, Zhang Y, Karakashev DB, Wang J, Angelidaki I. Biological caproate production by Clostridium kluyveri from ethanol and acetate as carbon sources. Bioresour Technol, 2017, 241: 638-644.

[42] Yong YC, Yu YY, Zhang X, Song H. Highly active bidirectional electron transfer by a self-assembled electroactive reduced-graphene-oxide-hybridized biofilm. Angew Chem, 2014, 53: 4480-4483.

[43] Zhang T, Nie HR, Bain TS, Lu HY, Cui MM, Snoeyenbos-West OL, Franks AE, Nevin KP, Russell TP, Lovley DR. Improved cathode materials for microbial electrosynthesis. Energy Environ Sci, 2013, 6: 217-224.

[44] Zhu ZG, Guo T, Zheng HJ, Song TS, Ouyang PK, Xie JJ. Complete genome sequence of a malodorant-producing acetogen, Clostridium scatologenes ATCC 25775(T). J Biotechnol, 2015, 212: 19-20.

Funding

the Major projects of natural science research in Jiangsu Province(15KJA530002)

the technology supporting program of Jiangsu Province(BE2015167)

the State Key Laboratory of Materials-Oriented Chemical Engineering(ZK201605)

Fund from the State Key Laboratory of Materials-Oriented Chemical Engineering(KL15-07)