Abiotic–Biological Hybrid Systems for CO₂ Conversion to Value-Added Chemicals and Fuels

Abstract

Abiotic–biological hybrid systems that combine the advantages of abiotic catalysis and biotransformation for the conversion of carbon dioxide (CO₂) to value-added chemicals and fuels have emerged as an appealing way to address the global energy and environmental crisis caused by increased CO₂ emission. We illustrate the recent progress in this field. Here, we first review the natural CO₂ fixation pathways for an in-depth understanding of the biological CO₂ transformation strategy and why a sustainable feed of reducing power is important. Second, we review the recent progress in the construction of abiotic–biological hybrid systems for CO₂ transformation from two aspects: (i) microbial electrosynthesis systems that utilize electricity to support whole-cell biological CO₂ conversion to products of interest and (ii) photosynthetic semiconductor biohybrid systems that integrate semiconductor nanomaterials with CO₂-fixing microorganisms to harness solar energy for biological CO₂ transformation. Lastly, we discuss potential approaches for further improvement of abiotic–biological hybrid systems.

Keywords

CO₂ conversion / Abiotic–biological hybrid systems / Microbial electrosynthesis systems / Photosynthetic semiconductor biohybrid systems

References

[1] Gong FY, Li Y. Fixing carbon, unnaturally. Science, 2016, 354(6314): 830-831.

[2] Mondal M, Goswami S, Ghosh A, et al. Production of biodiesel from microalgae through biological carbon capture: a review. Biotech, 2017, 7(2): 99.

[3] Adams S, Nsiah C. Reducing carbon dioxide emissions; does renewable energy matter?. Sci Total Environ, 2019, 693: 133288.

[4] Cheng J, Lu HX, He X, et al. Mutation of Spirulina sp. by nuclear irradiation to improve growth rate under 15% carbon dioxide in flue gas. Bioresour Technol, 2017, 238: 650-656.

[5] Singh HM, Kothari R, Gupta R, et al. Bio-fixation of flue gas from thermal power plants with algal biomass: overview and research perspectives. J Environ Manage, 2019, 245: 519-539.

[6] Liao JC, Mi L, Pontrelli S, et al. Fuelling the future: microbial engineering for the production of sustainable biofuels. Nat Rev Microbiol, 2016, 14(5): 288-304.

[7] Pacala S. Stabilization wedges: solving the climate problem for the next 50 years with current technologies. Science, 2004, 305(5686): 968-972.

[8] O'Neill BC, Oppenheimer M. Dangerous climate impacts and the Kyoto Protocol. Science, 2002, 296(5575): 1971-1972.

[9] Cuéllar-Franca RM, Azapagic A. Carbon capture, storage and utilisation technologies: a critical analysis and comparison of their life cycle environmental impacts. J CO2 Util, 2015, 9: 82-102.

[10] Songolzadeh M, Soleimani M, Takht Ravanchi M, et al. Carbon dioxide separation from flue gases: a technological review emphasizing reduction in greenhouse gas emissions. Sci World J, 2014, 2014: 828131.

[11] Bruhn T, Naims H, Olfe-Kräutlein B. Separating the debate on CO₂ utilisation from carbon capture and storage. Environ Sci Policy, 2016, 60: 38-43.

[12] Armstrong K, Styring P. Assessing the potential of utilization and storage strategies for post-combustion CO₂ emissions reduction. Front Energy Res, 2015, 3: 8.

[13] Stephens JC. Time to stop investing in carbon capture and storage and reduce government subsidies of fossil-fuels. WIREs Clim Change, 2014, 5(2): 169-173.

[14] Hepburn C, Adlen E, Beddington J, et al. The technological and economic prospects for CO₂ utilization and removal. Nature, 2019, 575(7781): 87-97.

[15] Fu ZY, Yang Q, Liu Z, et al. Photocatalytic conversion of carbon dioxide: from products to design the catalysts. J CO2 Util, 2019, 34: 63-73.

[16] Tan X, Huang XS, Zou YL, et al. Synthesis and characterization of Co-doped brookite titania photocatalysts with high photocatalytic activity. Trans Tianjin Univ, 2018, 24(2): 111-122.

[17] Liu JP, Peng WC, Li Y, et al. 2D MXene-based materials for electrocatalysis. Trans Tianjin Univ, 2020, 26(3): 149-171.

[18] Ross MB, de Luna P, Li YF, et al. Designing materials for electrochemical carbon dioxide recycling. Nat Catal, 2019, 2(8): 648-658.

[19] Appel AM, Bercaw JE, Bocarsly AB, et al. Frontiers, opportunities, and challenges in biochemical and chemical catalysis of CO₂ fixation. Chem Rev, 2013, 113(8): 6621-6658.

[20] Zhu M, Ge QF, Zhu XL. Catalytic reduction of CO₂ to CO via reverse water gas shift reaction: recent advances in the design of active and selective supported metal catalysts. Trans Tianjin Univ, 2020, 26(3): 172-187.

[21] Li ZH, Zhang LJ, Zhao KC, et al. Ni/ZrO₂ catalysts synthesized via urea combustion method for CO₂ methanation. Trans Tianjin Univ, 2018, 24(5): 471-479.

[22] Wong TS. Carbon dioxide capture and utilization using biological systems: opportunities and challenges. J Bioprocess Biotech, 2014, 4(3): 10.

[23] Zhao YF, Zhao YX, Waterhouse GIN, et al. Layered-double-hydroxide nanosheets as efficient Visible-light-driven photocatalysts for dinitrogen fixation. Adv Mater, 2017, 29(42): 1703828.

[24] Shi R, Waterhouse GIN, Zhang TR. Recent progress in photocatalytic CO₂ reduction over perovskite oxides. Solar RRL, 2017, 1(11): 1700126.

[25] Kumaravel V, Bartlett J, Pillai SC. Photoelectrochemical conversion of carbon dioxide (CO₂) into fuels and value-added products. ACS Energy Lett, 2020, 5(2): 486-519.

[26] Zhang L, Zhao ZJ, Gong JL. Nanostructured materials for heterogeneous electrocatalytic CO₂ reduction and their related reaction mechanisms. Angew Chem Int Ed, 2017, 56(38): 11326-11353.

[27] Zhou YJ, Kerkhoven EJ, Nielsen J. Barriers and opportunities in bio-based production of hydrocarbons. Nat Energy, 2018, 3(11): 925-935.

[28] Liu ZH, Wang K, Chen Y, et al. Third-generation biorefineries as the means to produce fuels and chemicals from CO₂. Nat Catal, 2020, 3(3): 274-288.

[29] Sakimoto KK, Kornienko N, Yang PD, et al. Cyborgian material design for solar fuel production: the emerging photosynthetic biohybrid systems. Acc Chem Res, 2017, 50(3): 476-481.

[30] Suastegui M, Matthiesen JE, Carraher JM, et al. Combining metabolic engineering and electrocatalysis: application to the production of polyamides from sugar. Angew Chem Int Ed, 2016, 55(7): 2368-2373.

[31] Lu AH, Li Y, Jin S, et al. Growth of non-phototrophic microorganisms using solar energy through mineral photocatalysis. Nat Commun, 2012, 3: 768.

[32] Gong FY, Cai Z, Li Y. Synthetic biology for CO₂ fixation. Sci China Life Sci, 2016, 59(11): 1106-1114.

[33] Bassham JA, Benson AA, Kay LD, et al. The path of carbon in photosynthesis. XXI. The cyclic regeneration of carbon dioxide acceptor. J Am Chem Soc, 1954, 76(7): 1760-1770.

[34] Ivanovsky RN, Fal YI, Berg IA, et al. Evidence for the presence of the reductive pentose phosphate cycle in a filamentous anoxygenic photosynthetic bacterium, Oscillochloris trichoides strain DG-6. Microbiology, 1999, 145(7): 1743-1748.

[35] Fuhrmann S, Ferner M, Jeffke T, et al. Complete nucleotide sequence of the circular megaplasmid pHCG3 of Oligotropha carboxidovorans: function in the chemolithoautotrophic utilization of CO, H₂ and CO₂. Gene, 2003, 322: 67-75.

[36] Berberoğlu H, Barra N, Pilon L, et al. Growth, CO₂ consumption and H₂ production of Anabaena variabilis ATCC 29413-U under different irradiances and CO₂ concentrations. J Appl Microbiol, 2007, 104(1): 105-121.

[37] Whitney SM, Houtz RL, Alonso H. Advancing our understanding and capacity to engineer nature's CO₂-sequestering enzyme. Rubisco Plant Physiol, 2011, 155(1): 27-35.

[38] Tcherkez GGB, Farquhar GD, Andrews TJ. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci USA, 2006, 103(19): 7246-7251.

[39] Ducat DC, Silver PA. Improving carbon fixation pathways. Curr Opin Chem Biol, 2012, 16(3–4): 337-344.

[40] Evans MC, Buchanan BB, Arnon DI. A new ferredoxin-dependent carbon reduction cycle in a photosynthetic bacterium. Proc Natl Acad Sci USA, 1966, 55(4): 928-934.

[41] Aoshima M, Ishii M, Igarashi Y. A novel enzyme, citryl-CoA lyase, catalysing the second step of the citrate cleavage reaction in Hydrogenobacter thermophilus TK-6. Mol Microbiol, 2004, 52(3): 763-770.

[42] Ikeda T, Ochiai T, Morita S, et al. Anabolic five subunit-type pyruvate:ferredoxin oxidoreductase from Hydrogenobacter thermophilus TK-6. Biochem Biophys Res Commun, 2006, 340(1): 76-82.

[43] Ljungdahl L, Irion E, Wood HG. Total synthesis of acetate from CO₂. I. Co-methylcobyric acid and Co-(methyl)-5-methoxybenzimidazolylcobamide as intermediates with Clostridium thermoaceticum. Biochemistry, 1965, 4(12): 2771-2780.

[44] Wood HG. Life with CO or CO₂ and H₂ as a source of carbon and energy. FASEB J, 1991, 5(2): 156-163.

[45] Thauer RK. A fifth pathway of carbon fixation. Science, 2007, 318(5857): 1732-1733.

[46] Ragsdale SW, Clark JE, Ljungdahl LG, et al. Properties of purified carbon monoxide dehydrogenase from Clostridium thermoaceticum, a nickel, iron-sulfur protein. J Biol Chem, 1983, 258(4): 2364-2369.

[47] Herter S, Fuchs G, Bacher A, et al. A bicyclic autotrophic CO₂ fixation pathway in Chloroflexus aurantiacus. J Biol Chem, 2002, 277(23): 20277-20283.

[48] Eisenreich W, Strauss G, Werz U, et al. Retrobiosynthetic analysis of carbon fixation in the phototrophic Eubacterium Chloroflexus aurantiacus. Eur J Biochem, 1993, 215(3): 619-632.

[49] Alber BE, Fuchs G. Propionyl-coenzyme A synthase from Chloroflexus aurantiacus, a key enzyme of the 3-hydroxypropionate cycle for autotrophic CO₂ fixation. J Biol Chem, 2002, 277(14): 12137-12143.

[50] Berg IA, Kockelkorn D, Buckel W, et al. A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science, 2007, 318(5857): 1782-1786.

[51] Teufel R, Kung JW, Kockelkorn D, et al. 3-hydroxypropionyl-coenzyme A dehydratase and acryloyl-coenzyme A reductase enzymes of the autotrophic 3-hydroxypropionate/4-hydroxybutyrate cycle in the sulfolobales. J Bacteriol, 2009, 191(14): 4572-4581.

[52] Huber H, Gallenberger M, Jahn U, et al. A dicarboxylate /4-hydroxybutyrate autotrophic carbon assimilation cycle in the hyperthermophilic Archaeum Ignicoccus hospitalis. Proc Natl Acad Sci USA, 2008, 105(22): 7851-7856.

[53] Ramos-Vera WH, Berg IA, Fuchs G. Autotrophic carbon dioxide assimilation in thermoproteales revisited. J Bacteriol, 2009, 191(13): 4286-4297.

[54] Nevin KP, Woodard TL, Franks AE, et al. Microbial electrosynthesis: feeding microbes electricity to convert carbon dioxide and water to multicarbon extracellular organic compounds. mBio, 2010, 1(2): e00103-e110.

[55] Nevin KP, Hensley SA, Franks AE, et al. Electrosynthesis of organic compounds from carbon dioxide is catalyzed by a diversity of acetogenic microorganisms. Appl Environ Microbiol, 2011, 77(9): 2882-2886.

[56] Faraghiparapari N, Zengler K. Production of organics from CO₂ by microbial electrosynthesis (MES) at high temperature. J Chem Technol Biotechnol, 2017, 92(2): 375-381.

[57] Rabaey K, Rozendal RA. Microbial electrosynthesis-revisiting the electrical route for microbial production. Nat Rev Microbiol, 2010, 8(10): 706-716.

[58] Li H, Opgenorth PH, Wernick DG, et al. Integrated electromicrobial conversion of CO₂ to higher alcohols. Science, 2012, 335(6076): 1596.

[59] Liu C, Colón BC, Ziesack M, et al. Water splitting-biosynthetic system with CO₂ reduction efficiencies exceeding photosynthesis. Science, 2016, 352(6290): 1210-1213.

[60] Rodrigues RM, Guan X, Iñiguez JA, et al. Perfluorocarbon nanoemulsion promotes the delivery of reducing equivalents for electricity-driven microbial CO₂ reduction. Nat Catal, 2019, 2(5): 407-414.

[61] Chen XL, Cao YX, Li F, et al. Enzyme-assisted microbial electrosynthesis of poly(3-hydroxybutyrate) via CO₂ bioreduction by engineered Ralstonia eutropha. ACS Catal, 2018, 8(5): 4429-4437.

[62] Kornienko N, Zhang JZ, Sakimoto KK, et al. Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis. Nat Nanotech, 2018, 13(10): 890-899.

[63] Liu C, Gallagher JJ, Sakimoto KK, et al. Nanowire-bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals. Nano Lett, 2015, 15(5): 3634-3639.

[64] Sakimoto KK, Wong AB, Yang P. Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science, 2016, 351(6268): 74-77.

[65] Kornienko N, Sakimoto KK, Herlihy DM, et al. Spectroscopic elucidation of energy transfer in hybrid inorganic–biological organisms for solar-to-chemical production. Proc Natl Acad Sci USA, 2016, 113(42): 11750-11755.

[66] Zhang RT, He Y, Yi J, et al. Proteomic and metabolic elucidation of solar-powered biomanufacturing by bio-abiotic hybrid system. Chem, 2020, 6(1): 234-249.

[67] Zhang H, Liu H, Tian ZQ, et al. Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production. Nat Nanotech, 2018, 13(10): 900-905.

[68] Gai PP, Yu W, Zhao H, et al. Solar-powered organic semiconductor-bacteria biohybrids for CO₂ reduction into acetic acid. Angew Chem Int Ed, 2020, 59(18): 7224-7229.

[69] Ding YC, Bertram JR, Eckert C, et al. Nanorg microbial factories: light-driven renewable biochemical synthesis using quantum dot-bacteria nanobiohybrids. J Am Chem Soc, 2019, 141(26): 10272-10282.

[70] Xu MY, Tremblay PL, Jiang LL, et al. Stimulating bioplastic production with light energy by coupling Ralstonia eutropha with the photocatalyst graphitic carbon nitride. Green Chem, 2019, 21(9): 2392-2400.

[71] Tremblay PL, Xu MY, Chen YM, et al. Nonmetallic abiotic-biological hybrid photocatalyst for visible water splitting and carbon dioxide reduction. iScience, 2020, 23(1): 100784.