Semi-Biological Approaches to Solar-To-Chemical Conversion Cite This: Chem
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Chem Soc Rev View Article Online REVIEW ARTICLE View Journal | View Issue Semi-biological approaches to solar-to-chemical conversion Cite this: Chem. Soc. Rev., 2020, 49,4926 Xin Fang, Shafeer Kalathil and Erwin Reisner * This review presents a comprehensive summary of the recent development in semi-artificial photosynthesis, a biological-material hybrid approach to solar-to-chemical conversion that provides new concepts to shape a sustainable future fuelled by solar energy. We begin with a brief introduction to natural and artificial photosynthesis, followed by a discussion of the motivation and rationale behind semi-artificial photosynthesis. Then, we summarise how various enzymes can be combined with synthetic materials for light-driven water oxidation, H2 evolution, Received 28th October 2019 CO2 reduction, and chemical synthesis more broadly. In the following section, we discuss the strategies to DOI: 10.1039/c9cs00496c incorporate microorganisms in photocatalytic and (photo)electrochemical systems to produce fuels and chemicals with renewable sources. Finally, we outline emerging analytical techniques to study the bio-material hybrid rsc.li/chem-soc-rev systems and propose unexplored research opportunities in the field of semi-artificial photosynthesis. Creative Commons Attribution 3.0 Unported Licence. 1 Introduction catalysts still encounter challenges in solar-to-chemical conversion, nature provides evolutionarily-optimised biocatalysts. This review The consequences of anthropogenic carbon emissions call for summarises how this biological machinery can be leveraged to innovative strategies to develop renewable energy technologies. catalyse light-driven reactions by an emerging technology termed Photovoltaics (PV) is the leading technology for solar energy ‘‘semi-artificial photosynthesis’’, in which biocatalysts in the form of conversion,1,2 butitshowsdisadvantagesinintermittencyand enzymes or microorganisms are incorporated with particles or long-distance electricity transmission. Artificial photosynthesis is a structurally-crafted electrodes to produce fuels or chemicals. This article is licensed under a process that converts solar energy into fuels and it thereby circum- ventsthesedrawbacksbystoringsolar energy in chemical bonds 1.1 Natural photosynthesis using synthetic light absorbers and catalysts.3,4 While synthetic Open Access Article. Published on 15 June 2020. Downloaded 10/10/2021 5:24:44 PM. Photosynthesis occurs in photoautotrophs such as cyanobacteria, Department of Chemistry, University of Cambridge, Lensfield Road, Cambridge CB2 algae and higher plants, which harvest solar energy to produce 1EW, UK. E-mail: [email protected] biomass and O2 from CO2 and H2O. Photosynthesis is accomplished Xin Fang obtained his PhD degree Shafeer Kalathil obtained his PhD in from the University of Cambridge Chemical Engineering at Yeungnam under the supervision of Prof. Erwin University under the supervision of Reisner. His doctoral research Prof. Moo Hwan Cho, where he focused on establishing efficient worked on microbial fuel cells and solar-to-chemical conversion avenues microbialcellfactories.Hewasa with biocatalysts in the form of JSPS Fellow at the University of enzymes and whole cells. His Tokyo (with Prof. Kazuhito research broadly traverses the fields Hashimoto) and a Postdoctoral of biocatalysis, materials science, Fellow at KAUST (with Prof. Pascal electrochemistry, and photocata- Saikaly). He joined the group of lysis, with the aim to shift the Prof. Erwin Reisner (University of Xin Fang paradigm of artificial photo- Shafeer Kalathil Cambridge) as a Marie Curie synthesis by rationally integrating Fellow to work on the microbial biocatalysts with synthetic components. Before that, he studied at electrosynthesis of value-added products from waste-carbon. His current Fudan University and Sichuan University for a Master and Bachelor’s research focuses on the integration of light-harvesting materials with degree in polymer science, respectively. microbes to produce industrially relevant chemicals from carbon dioxide. 4926 | Chem. Soc. Rev., 2020, 49, 4926--4952 This journal is © The Royal Society of Chemistry 2020 View Article Online Review Article Chem Soc Rev by two phases of reactions: the light reaction uses solar energy to generate the energy carrier adenosine triphosphate (ATP) and the reduced nicotinamide adenine dinucleotide phosphate (NADPH) as the reducing agent; the dark reaction then uses the ATP and NADPH to reduce atmospheric CO2 into carbohydrates through the Calvin cycle.5 1.1.1 Light reactions. The light reaction is carried out in the thylakoid membrane by the photosynthetic apparatus, including photosystem II (PSII) and photosystem I (PSI), cyto- chrome b6 f (cyt b6 f ), the plastoquinone (PQ) pool, plastocyanin (PC), ferredoxin (Fd), ferredoxin–NADP+ reductase (FNR) and ATP synthase (ATPase) (Fig. 1a).6 The two light absorbing photosystems both contain antenna complexes and reaction centres. The antenna complex comprises hundreds of pigments (chlorophylls and carotenoids), which capture photons and funnel the light energy to the reaction centre at a high quantum efficiency of 495%. The reaction centre is a transmembrane protein–pigment complex, where electrons are excited and transferred to the downstream chemical synthesis pathway. The reaction centre chlorophylls in PSII and PSI are referred to as P680 and P700, respectively. The two photosystems function in concert to efficiently transfer electrons from H2O + Creative Commons Attribution 3.0 Unported Licence. to NADP through a ‘‘Z-scheme’’ (Fig. 1b). The electron transfer in the thylakoid membrane is initiated by PSII, which absorbs photons and extracts electrons from H2O to reduce its terminal electron acceptor, plastoquinone B (QB). The fully reduced Fig. 1 Schematic illustration of the light reaction in natural photo- synthesis. (a) Electron and proton transfer pathways in the thylakoid plastohydroquinone (QBH2) dissociates from the reaction cen- membrane. At the start of the photosynthetic chain is PSII that oxidises tre and transfers its electrons to cyt b6 f, which forwards the H O and releases O and protons upon light absorption. The electrons are electrons to PSI via a small copper-containing protein PC. At 2 2 then delivered to PSI via a plastoquinone (PQ) pool, cyt b6f and plasto- PSI, the arriving electrons are energised by a second excitation cyanin (PC). Electrons are photoexcited for a second time at PSI to reduce and finally delivered to FNR to reduce NADP+ to NADPH NADP+ to NADPH via a ferredoxin (Fd) and a ferredoxin–NADP+ reductase This article is licensed under a (Fig. 1a).5 Simultaneously, the water oxidation and the electron (FNR). The water oxidation and electron transport also induce proton transport induce proton translocation from the stroma to the translocation from the stroma to the lumen, which generates a proton gradient and chemiosmosis driving the synthesis of ATP by ATP synthase lumen, which generates a proton gradient and chemiosmosis (ATPase). Protein data bank ID: PSII (4ub6), cyt b6f (4h44), PC (1bxu), PSI Open Access Article. Published on 15 June 2020. Downloaded 10/10/2021 5:24:44 PM. driving the synthesis of ATP by ATPase. (5oy0), Fd-FNR (2yvj), ATPase (6fkf). (b) Energy level diagram of the Z-scheme electron transfer in the thylakoid membrane. The redox carriers are placed at their midpoint redox potentials at pH 7.0. Erwin Reisner received his PhD 1.1.2 Dark reactions. The NADPH and ATP produced by the degree from the University of light reaction are then used to reduce CO2 to carbohydrates in Vienna (with Prof. Bernhard K. the Calvin cycle. During the process, CO2 and H2O are com- Keppler), and postdoctoral training bined with the carbon acceptor ribulose-1,5-bisphosphate to at the Massachusetts Institute of yield two molecules of 3-phosphoglycerate. This intermediate is Technology (with Prof. Stephen then reduced to glyceraldehyde-3-phosphate with ATP and J. Lippard) and the University of NADPH. The cycle closes with the regeneration of ribulose-1,5- 6 Oxford (with Prof. Fraser A. bisphosphate, the initial CO2 acceptor. The Calvin cycle accounts Armstrong) in biological inorganic for more than 90% of carbon assimilation on earth. Central to chemistry, before moving to the this reaction is ribulose-1,5-bisphosphate carboxylase/oxygenase 7,8 University of Cambridge where he (Rubisco) that covalently fixes CO2 to a carbon skeleton. Rubisco is currently the Professor of Energy is abundant in nature and operates using atmospheric CO2 con- B Erwin Reisner and Sustainability. His laboratory centrations ( 415 ppm). However, it also displays slow catalysis explores the interface of chemical and low selectivity. The turnover frequency (TOF) of Rubisco is À1 biology, synthetic chemistry, materials science and engineering relevant typically less than 10 s , rendering the photosynthetic CO2 to the development of solar-driven processes for the sustainable synthesis fixation inefficient under optimal conditions.8 It also confuses of fuels and chemicals. the substrate (CO2) and the product (O2) of photosynthesis, This journal is © The Royal Society of Chemistry 2020 Chem. Soc. Rev., 2020, 49, 4926--4952 | 4927 View Article Online Chem Soc Rev Review Article which offsets the CO2 uptake and saddles oxygenic phototrophs feedstock chemicals such as H2O and CO2. A prototype reaction 9 with energy-dissipating photorespiration. is light-driven water splitting, which produces H2 as a suitable Photorespiration can consume