Material–Microbe Interfaces for Solar-Driven CO2 Bioelectrosynthesis
2020; Elsevier BV; Volume: 38; Issue: 11 Linguagem: Inglês
10.1016/j.tibtech.2020.03.008
ISSN0167-9430
AutoresPrakash C. Sahoo, Deepak Pant, Manoj Kumar, S.K. Puri, S.S.V. Ramakumar,
Tópico(s)Advanced Photocatalysis Techniques
ResumoMany self-photosensitized bioinorganic hybrid systems have recently been developed by exploiting material–microbe interactions. These hybrids combine the complex functionality of biological systems and inorganic materials to efficiently catalyze the photoreduction of CO2 to chemicals and fuel precursors.The multifaceted mechanism of material–microbe interactions depends on several factors, including the band-gap of the material, biomineralization strategy, biocompatibility, nature of membrane-bound proteins, and electron carriers.Well-organized biohybrid materials can be used to develop bio-inspired materials for biomedical and therapeutic applications. Genetically improving microbes can further improve the biohybrid performance. Sustainable production of solar-based chemicals is possible by mimicking the natural photosynthetic mechanism. To realize the full potential of solar-to-chemical production, the artificial means of photosynthesis and the biological approach should complement each other. The recently developed hybrid microbe–metal interface combines an inorganic, semiconducting light-harvester material with efficient and simple microorganisms, resulting in a novel metal–microbe interface that helps the microbes to capture energy directly from sunlight. This solar energy is then used for sustainable biosynthesis of chemicals from CO2. This review discusses various approaches to improve the electron uptake by microbes at the bioinorganic interface, especially self-photosensitized microbial systems and integrated water splitting biosynthetic systems, with emphasis on CO2 bioelectrosynthesis. Sustainable production of solar-based chemicals is possible by mimicking the natural photosynthetic mechanism. To realize the full potential of solar-to-chemical production, the artificial means of photosynthesis and the biological approach should complement each other. The recently developed hybrid microbe–metal interface combines an inorganic, semiconducting light-harvester material with efficient and simple microorganisms, resulting in a novel metal–microbe interface that helps the microbes to capture energy directly from sunlight. This solar energy is then used for sustainable biosynthesis of chemicals from CO2. This review discusses various approaches to improve the electron uptake by microbes at the bioinorganic interface, especially self-photosensitized microbial systems and integrated water splitting biosynthetic systems, with emphasis on CO2 bioelectrosynthesis. Increasing CO2 concentration, due to anthropogenic activities, is believed to have a serious impact on climate. 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Solar-driven bioelectrosynthesis through the microbe–material interface is an emerging artificial photosynthesis system that combines the strengths of inorganic materials and living microbial cells to achieve a solar energy conversion efficiency of ~20% with high selectivity towards CO2-to-chemicals [27.Cestellos-Blanco S. et al.Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids.Faraday Discuss. 2019; 215: 54-65Crossref PubMed Google Scholar,29.Kornienko N. et al.Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis.Nat. Nanotechnol. 2018; 13: 890-899Crossref PubMed Scopus (206) Google Scholar, 30.Dogutan D.K. Nocera D.G. Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis.Acc. Chem. Res. 2019; 52: 3143-3148Crossref PubMed Scopus (95) Google Scholar, 31.Lin J. et al.Regulations of organism by materials: a new understanding of biological inorganic chemistry.JBIC J. Biol. Inorg. Chem. 2019; 24: 467-481Crossref Scopus (11) Google Scholar, 32.Zhang B. Sun L. Artificial photosynthesis: opportunities and challenges of molecular catalysts.Chem. Soc. Rev. 2019; 48: 2216-2264Crossref PubMed Google Scholar, 33.Sakimoto K.K. et al.Physical biology of the materials–microorganism interface.J. Am. Chem. Soc. 2018; 140: 1978-1985Crossref PubMed Scopus (88) Google Scholar]. Such self-photosensitizing systems accompany living systems with light-absorbing materials (in nano, micro, or macro dimensions) and act as chemical factories (Box 1).Box 1Advantages of Self-Photosensitized Bioinorganic Hybrid Systems over MESMES is a promising approach to obtain fuels and chemicals from CO2 using renewable energy sources. In an MES, microorganisms accept electrons from a cathode to reduce CO2 to form organic compounds [21.del Pilar Anzola Rojas M. et al.Effect of the electric supply interruption on a microbial electrosynthesis system converting inorganic carbon into acetate.Bioresour. Technol. 2018; 266: 203-210Crossref PubMed Scopus (69) Google Scholar,22.del Pilar Anzola Rojas M. et al.Microbial electrosynthesis (MES) from CO2 is resilient to fluctuations in renewable energy supply.Energy Convers. Manag. 2018; 177: 272-279Crossref Scopus (81) Google Scholar]. One of the challenges in an MES-based system is the design of the reactor for scale-up production. For instance, in an MES, the cathode potential has to be controlled precisely to prevent the production of H2 and to avoid cell damage. Further, the membrane between the anode chamber and cathode chamber, designed to permit ion flux and restrict oxygen diffusion, also adds cost. Finally, the extracellular interaction between the living cell membranes of microbes and the electrode, as well as the inability of these microbes to cope with the intermittent nature of renewable electricity (mainly from solar, wind, and tidal currents) and electron losses due to various factors like sluggish kinetics of charge transfer need to be addressed [25.Rabaey K. Rozendal R.A. Microbial electrosynthesis—revisiting the electrical route for microbial production.Nat. Rev. Microbiol. 2010; 8: 706Crossref PubMed Scopus (1057) Google Scholar, 26.Batlle-Vilanova P. et al.Continuous acetate production through microbial electrosynthesis from CO2 with microbial mixed culture.J. Chem. Technol. Biotechnol. 2016; 91: 921-927Crossref Scopus (99) Google Scholar, 27.Cestellos-Blanco S. et al.Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids.Faraday Discuss. 2019; 215: 54-65Crossref PubMed Google Scholar].Solar-driven bioelectrosynthesis, however, relies on the microbe–material interface. During this process, nonphotosynthetic microorganisms are sensitized by providing them with energy in the form of reducing equivalents from an efficient light-absorbing inorganic or organic light harvester [27.Cestellos-Blanco S. et al.Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids.Faraday Discuss. 2019; 215: 54-65Crossref PubMed Google Scholar, 28.Royanian S. et al.Efficiency enhancement of ultra-thin CIGS solar cells using bandgap grading and embedding Au plasmonic nanoparticles.Plasmonics. 2020; 15: 1173-1182Crossref Scopus (18) Google Scholar, 29.Kornienko N. et al.Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis.Nat. Nanotechnol. 2018; 13: 890-899Crossref PubMed Scopus (206) Google Scholar, 30.Dogutan D.K. Nocera D.G. Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis.Acc. Chem. Res. 2019; 52: 3143-3148Crossref PubMed Scopus (95) Google Scholar, 31.Lin J. et al.Regulations of organism by materials: a new understanding of biological inorganic chemistry.JBIC J. Biol. Inorg. Chem. 2019; 24: 467-481Crossref Scopus (11) Google Scholar, 32.Zhang B. Sun L. Artificial photosynthesis: opportunities and challenges of molecular catalysts.Chem. Soc. Rev. 2019; 48: 2216-2264Crossref PubMed Google Scholar, 33.Sakimoto K.K. et al.Physical biology of the materials–microorganism interface.J. Am. Chem. Soc. 2018; 140: 1978-1985Crossref PubMed Scopus (88) Google Scholar]. The biohybrid system acts as a self-sustaining chemical factory. Moreover, the hybrid system is self-regenerating, with low waste generation, and it operates at an efficiency (product yield based on solar energy input) of more than 80% [27.Cestellos-Blanco S. et al.Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids.Faraday Discuss. 2019; 215: 54-65Crossref PubMed Google Scholar, 28.Royanian S. et al.Efficiency enhancement of ultra-thin CIGS solar cells using bandgap grading and embedding Au plasmonic nanoparticles.Plasmonics. 2020; 15: 1173-1182Crossref Scopus (18) Google Scholar, 29.Kornienko N. et al.Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis.Nat. Nanotechnol. 2018; 13: 890-899Crossref PubMed Scopus (206) Google Scholar, 30.Dogutan D.K. Nocera D.G. Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis.Acc. Chem. Res. 2019; 52: 3143-3148Crossref PubMed Scopus (95) Google Scholar, 31.Lin J. et al.Regulations of organism by materials: a new understanding of biological inorganic chemistry.JBIC J. Biol. Inorg. Chem. 2019; 24: 467-481Crossref Scopus (11) Google Scholar, 32.Zhang B. Sun L. Artificial photosynthesis: opportunities and challenges of molecular catalysts.Chem. Soc. Rev. 2019; 48: 2216-2264Crossref PubMed Google Scholar, 33.Sakimoto K.K. et al.Physical biology of the materials–microorganism interface.J. Am. Chem. Soc. 2018; 140: 1978-1985Crossref PubMed Scopus (88) Google Scholar]. MES is a promising approach to obtain fuels and chemicals from CO2 using renewable energy sources. In an MES, microorganisms accept electrons from a cathode to reduce CO2 to form organic compounds [21.del Pilar Anzola Rojas M. et al.Effect of the electric supply interruption on a microbial electrosynthesis system converting inorganic carbon into acetate.Bioresour. Technol. 2018; 266: 203-210Crossref PubMed Scopus (69) Google Scholar,22.del Pilar Anzola Rojas M. et al.Microbial electrosynthesis (MES) from CO2 is resilient to fluctuations in renewable energy supply.Energy Convers. Manag. 2018; 177: 272-279Crossref Scopus (81) Google Scholar]. One of the challenges in an MES-based system is the design of the reactor for scale-up production. For instance, in an MES, the cathode potential has to be controlled precisely to prevent the production of H2 and to avoid cell damage. Further, the membrane between the anode chamber and cathode chamber, designed to permit ion flux and restrict oxygen diffusion, also adds cost. Finally, the extracellular interaction between the living cell membranes of microbes and the electrode, as well as the inability of these microbes to cope with the intermittent nature of renewable electricity (mainly from solar, wind, and tidal currents) and electron losses due to various factors like sluggish kinetics of charge transfer need to be addressed [25.Rabaey K. Rozendal R.A. Microbial electrosynthesis—revisiting the electrical route for microbial production.Nat. Rev. Microbiol. 2010; 8: 706Crossref PubMed Scopus (1057) Google Scholar, 26.Batlle-Vilanova P. et al.Continuous acetate production through microbial electrosynthesis from CO2 with microbial mixed culture.J. Chem. Technol. Biotechnol. 2016; 91: 921-927Crossref Scopus (99) Google Scholar, 27.Cestellos-Blanco S. et al.Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids.Faraday Discuss. 2019; 215: 54-65Crossref PubMed Google Scholar]. Solar-driven bioelectrosynthesis, however, relies on the microbe–material interface. During this process, nonphotosynthetic microorganisms are sensitized by providing them with energy in the form of reducing equivalents from an efficient light-absorbing inorganic or organic light harvester [27.Cestellos-Blanco S. et al.Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids.Faraday Discuss. 2019; 215: 54-65Crossref PubMed Google Scholar, 28.Royanian S. et al.Efficiency enhancement of ultra-thin CIGS solar cells using bandgap grading and embedding Au plasmonic nanoparticles.Plasmonics. 2020; 15: 1173-1182Crossref Scopus (18) Google Scholar, 29.Kornienko N. et al.Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis.Nat. Nanotechnol. 2018; 13: 890-899Crossref PubMed Scopus (206) Google Scholar, 30.Dogutan D.K. Nocera D.G. Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis.Acc. Chem. Res. 2019; 52: 3143-3148Crossref PubMed Scopus (95) Google Scholar, 31.Lin J. et al.Regulations of organism by materials: a new understanding of biological inorganic chemistry.JBIC J. Biol. Inorg. Chem. 2019; 24: 467-481Crossref Scopus (11) Google Scholar, 32.Zhang B. Sun L. Artificial photosynthesis: opportunities and challenges of molecular catalysts.Chem. Soc. Rev. 2019; 48: 2216-2264Crossref PubMed Google Scholar, 33.Sakimoto K.K. et al.Physical biology of the materials–microorganism interface.J. Am. Chem. Soc. 2018; 140: 1978-1985Crossref PubMed Scopus (88) Google Scholar]. The biohybrid system acts as a self-sustaining chemical factory. Moreover, the hybrid system is self-regenerating, with low waste generation, and it operates at an efficiency (product yield based on solar energy input) of more than 80% [27.Cestellos-Blanco S. et al.Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids.Faraday Discuss. 2019; 215: 54-65Crossref PubMed Google Scholar, 28.Royanian S. et al.Efficiency enhancement of ultra-thin CIGS solar cells using bandgap grading and embedding Au plasmonic nanoparticles.Plasmonics. 2020; 15: 1173-1182Crossref Scopus (18) Google Scholar, 29.Kornienko N. et al.Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis.Nat. Nanotechnol. 2018; 13: 890-899Crossref PubMed Scopus (206) Google Scholar, 30.Dogutan D.K. Nocera D.G. Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis.Acc. Chem. Res. 2019; 52: 3143-3148Crossref PubMed Scopus (95) Google Scholar, 31.Lin J. et al.Regulations of organism by materials: a new understanding of biological inorganic chemistry.JBIC J. Biol. Inorg. Chem. 2019; 24: 467-481Crossref Scopus (11) Google Scholar, 32.Zhang B. Sun L. Artificial photosynthesis: opportunities and challenges of molecular catalysts.Chem. Soc. Rev. 2019; 48: 2216-2264Crossref PubMed Google Scholar, 33.Sakimoto K.K. et al.Physical biology of the materials–microorganism interface.J. Am. Chem. Soc. 2018; 140: 1978-1985Crossref PubMed Scopus (88) Google Scholar]. In a breakthrough development, Sakimoto and colleagues studied the efficacy of a Morella thermoacetica–cadmium sulfide (CdS) quantum dot hybrid to convert CO2 to chemicals under visible radiation [34.Sakimoto K.K. et al.Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production.Science. 2016; 351: 74-77Crossref PubMed Scopus (559) Google Scholar]. Thereafter, several hybrid photosynthesis systems were developed, where the metabolic adaptability of microbes was tailored by integrating light-harvesting inorganic materials to drive the bioelectrosynthesis of CO2 into fuels and chemicals [35.Liu C. et al.Nanowire–bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals.Nano Lett. 2015; 15: 3634-3639Crossref PubMed Scopus (273) Google Scholar, 36.Kumar M. et al.Photosensitization of electro-active microbes for solar assisted carbon dioxide transformation.Bioresour. 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Such hybrid photosynthesis systems are distinct as they can couple with numerous inorganic light-harvesting 2D or 3D materials, such as nanoparticles (NPs), quantum dots, nanowires (NWs), and biological catalysts, including enzymes and autotrophic or heterotrophic microbes [35.Liu C. et al.Nanowire–bacteria hybrids for unassisted solar carbon dioxide fixation to value-added chemicals.Nano Lett. 2015; 15: 3634-3639Crossref PubMed Scopus (273) Google Scholar, 36.Kumar M. et al.Photosensitization of electro-active microbes for solar assisted carbon dioxide transformation.Bioresour. 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Recent pioneering works have focused on various photosensitized microbial systems as well as integrated water splitting–biosynthetic systems to understand the entire solar–chemical pathway (Figure 1) [40.Liu C. et al.Solar-powered CO2 reduction by a hybrid biological inorganic system.J. Photochem. Photobiol. A Chem. 2018; 358: 411-415Crossref Scopus (20) Google Scholar, 41.Torella J.P. et al.Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system.Proc. Natl. Acad. Sci. U.S.A. 2015; 112: 2337-2342Crossref PubMed Scopus (249) Google Scholar, 42.Liu C. et al.Water splitting–biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis.Science. 2016; 352: 1210-1213Crossref PubMed Scopus (558) Google Scholar]. This review summarizes advances in the transfer of energy or signals at the interface between inorganic or organic material and whole-cell organisms to fix CO2 into fuels and chemicals. In solar-driven bioelectrosynthesis, inorganic sunlight absorbers capture solar energy and transfer reducing equivalents to biological systems to drive CO2 reduction. In the biological system, CO2 is converted via the Wood-Ljungdahl (WL) pathway [43.Ragsdale S.W. Pierce E. Acetogenesis and the Wood–Ljungdahl pathway of CO2 fixation.Biochim. Biophys. Acta Proteins Proteomics. 2008; 1784: 1873-1898Crossref Scopus (692) Google Scholar] (Figure 2). In the WL pathway, acetic acid is synthesized from CO2 by autotrophic and anaerobic microorganisms, including Proteobacteria, Planctomycetes, Spirochaetes, and Euryarchaeota. Such microorganisms use hydrogen as the electron donor and CO2 as the electron acceptor for the biosynthesis of cellular precursors through simultaneous oxidation and reduction of CO2. Sakimoto and colleagues studied the photoreductive ability of an M. thermoacetica–CdS hybrid under visible light [34.Sakimoto K.K. et al.Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production.Science. 2016; 351: 74-77Crossref PubMed Scopus (559) Google Scholar]. In this system, electron (e–) and hole (h+) pairs are generated by the absorption of visible light via CdS as a semiconducting light harvester. The photoinduced electrons generate CO2-reducing equivalent, [H+], which then passes through the WL pathway to produce acetic acid from CO2. The holes are quenched by cysteine molecules, leading to the formation of cystine (CySS), the oxidized form of cysteine. The overall equation is given here:2CO2+8Cysteine+8photon→CH3COOH+2H2O+4CySS[1] Ye and coworkers studied an exhaustive mechanistic model for photoreductive reactions in microbial systems to convert CO2 to methane [39.Ye J. et al.Light-driven carbon dioxide reduction to methane by Methanosarcina barkeri-CdS biohybrid.Appl. Catal. B Environ. 2019; 257: 117916Crossref Scopus (63) Google Scholar]. According to this model, electron transfer from an inorganic photosensitizer to the microbial cell is facilitated by membrane-bound proteins. Membrane-bound proteins like hydrogenases and cytochromes play a key role in electron transport during e–/h+ separation and facilitate the conversion of CO2 to CH4 [44.Shi L. et al.Extracellular electron transfer mechanisms between microorganisms and minerals.Nat. Rev. Microbiol. 2016; 14: 651Crossref PubMed Scopus (769) Google Scholar]. Further, various concentrations of proteinase K, an enzyme that exhibits specific cleavage and denaturation of membrane-bound proteins, were used to establish the importance of membrane-bound proteins in an Methanosarcina barkeri–CdS biohybrid system. The results suggested that with a rising concentration of proteinase K, the CO2 to CH4 conversion efficiency in M. barkeri–CdS biohybrid steadily decreased, which demonstrates the major role of membrane-bound proteins. Natural photosynthetic organisms are more selective than chemical catalysts for CO2 reduction to valuable chemicals, yet they are limited by extremely low efficiency [41.Torella J.P. et al.Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system.Proc. Natl. Acad. Sci. U.S.A. 2015; 112: 2337-2342Crossref PubMed Scopus (249) Google Scholar,42.Liu C. et al.Water splitting–biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis.Science. 2016; 352: 1210-1213Crossref PubMed Scopus (558) Google Scholar]. At the same time, using inorganic semiconducting materials, up to 20% solar energy conversion efficiency has been achieved against a maximum theoretical limit of 33.7% [28.Royanian S. et al.Efficiency enhancement of ultra-thin CIGS solar cells using bandgap grading and embedding Au plasmonic nanoparticles.Plasmonics.
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