DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Interfacing nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis

Journal Article · · Nature Nanotechnology
 [1]; ORCiD logo [2];  [3];  [4];  [2]
  1. Univ. of Cambridge (United Kingdom). Dept. of Chemistry; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry
  2. Univ. of Cambridge (United Kingdom). Dept. of Chemistry
  3. Univ. of Cambridge (United Kingdom). Dept. of Chemistry; Univ. of California, Berkeley, CA (United States). Dept. of Chemistry; Harvard Medical School, Boston, MA (United States). Dept. of Systems Biology
  4. Univ. of California, Berkeley, CA (United States). Dept. of Chemistry, and Dept. of Materials Science; Kavli Energy NanoSciences Inst., Berkeley, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Chemical Sciences Division

Semi-artificial photosynthetic systems aim to overcome the limitations of natural and artificial photosynthesis while providing an opportunity to investigate their respective functionality. The progress and studies of these hybrid systems is the focus of this forward-looking perspective. Enzymes have been interfaced with synthetic materials and employed for semi-artificial fuel production. In parallel, we examine how more complex living cellular systems can be recruited for in vivo fuel and chemical production in an approach where inorganic nanostructures are hybridized with photosynthetic and non-photosynthetic microorganisms. Side-by-side comparisons reveal strengths and limitations of enzyme- and microorganism-based hybrid systems, and how lessons extracted from studying enzyme hybrids can be applied to investigations of microorganism-hybrid devices. Here, we conclude by putting semi-artificial photosynthesis in the context of its own ambitions and discuss how it can help address the grand challenges facing artificial systems for the efficient generation of solar fuels and chemicals.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22), Chemical Sciences, Geosciences & Biosciences Division (SC-22.1)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1561899
Journal Information:
Nature Nanotechnology, Journal Name: Nature Nanotechnology Journal Issue: 10 Vol. 13; ISSN 1748-3387
Publisher:
Nature Publishing GroupCopyright Statement
Country of Publication:
United States
Language:
English

References (130)

Enhanced Biological Hydrogen Production from Escherichia coli with Surface Precipitated Cadmium Sulfide Nanoparticles journal July 2017
C-Type Cytochromes Wire Electricity-Producing Bacteria to Electrodes journal June 2008
Photocatalytic Hydrogen Evolution with a Hydrogenase in a Mediator-Free System under High Levels of Oxygen journal September 2013
Photocatalytic Hydrogen Production using Polymeric Carbon Nitride with a Hydrogenase and a Bioinspired Synthetic Ni Catalyst journal September 2014
Photoelectrochemical H 2 Evolution with a Hydrogenase Immobilized on a TiO 2 -Protected Silicon Electrode journal April 2016
Photoelectrochemical Reduction of Carbon Dioxide to Methanol through a Highly Efficient Enzyme Cascade journal January 2017
Solar Water Splitting with a Hydrogenase Integrated in Photoelectrochemical Tandem Cells journal August 2018
C-Type Cytochromes Wire Electricity-Producing Bacteria to Electrodes journal June 2008
In Situ Spectroelectrochemical Investigation of Electrocatalytic Microbial Biofilms by Surface-Enhanced Resonance Raman Spectroscopy journal February 2011
Editorial: The Nonsense of Biofuels journal February 2012
Combination of A Photosystem 1-Based Photocathode and a Photosystem 2-Based Photoanode to a Z-Scheme Mimic for Biophotovoltaic Applications journal November 2013
Photocatalytic Hydrogen Evolution with a Hydrogenase in a Mediator-Free System under High Levels of Oxygen journal September 2013
Photocatalytic Hydrogen Production using Polymeric Carbon Nitride with a Hydrogenase and a Bioinspired Synthetic Ni Catalyst journal September 2014
Photoelectrochemical H 2 Evolution with a Hydrogenase Immobilized on a TiO 2 -Protected Silicon Electrode journal April 2016
Photoelectrochemical Reduction of Carbon Dioxide to Methanol through a Highly Efficient Enzyme Cascade journal January 2017
Solar Water Splitting with a Hydrogenase Integrated in Photoelectrochemical Tandem Cells journal July 2018
Microalgae for the production of bulk chemicals and biofuels journal May 2010
Photoelectron Generation by Photosystem II Core Complexes Tethered to Gold Surfaces journal April 2010
Use of Bipolar Membranes for Maintaining Steady-State pH Gradients in Membrane-Supported, Solar-Driven Water Splitting journal September 2014
Photocurrent Generation from Thylakoid Membranes on Osmium-Redox-Polymer-Modified Electrodes journal February 2015
Sunlight-Dependent Hydrogen Production by Photosensitizer/Hydrogenase Systems journal February 2017
Photo-Induced Electron Transfer Between Photosystem 2 via Cross-linked Redox Hydrogels journal May 2008
How fast can Photosystem II split water? Kinetic performance at high and low frequencies journal June 2005
Marine phototrophic consortia transfer electrons to electrodes in response to reductive stress journal September 2015
Hydrogenase and its application for photoinduced hydrogen evolution journal December 1985
Oxygen-evolving complex of Photosystem II: an analysis of second-shell residues and hydrogen-bonding networks journal April 2015
Biological-inorganic hybrid systems as a generalized platform for chemical production journal December 2017
What is the maximum efficiency with which photosynthesis can convert solar energy into biomass? journal April 2008
Investigating the mechanism of thylakoid direct electron transfer for photocurrent generation journal April 2014
Solar-powered CO2 reduction by a hybrid biological | inorganic system journal May 2018
One-step electrosynthesis of ethylene and ethanol from CO2 in an alkaline electrolyzer journal January 2016
Photocurrent generation properties of Histag-photosystem II immobilized on nanostructured gold electrode journal March 2008
Metabolic engineering of cyanobacteria for photosynthetic 3-hydroxypropionic acid production from CO2 using Synechococcus elongatus PCC 7942 journal September 2015
[NiFeSe]-Hydrogenase Chemistry journal October 2015
Cyborgian Material Design for Solar Fuel Production: The Emerging Photosynthetic Biohybrid Systems journal March 2017
Solar Fuels and Solar Chemicals Industry journal March 2017
CO 2 Reduction Catalyzed by Nitrogenase: Pathways to Formate, Carbon Monoxide, and Methane journal August 2016
Role of Surface-Capping Ligands in Photoexcited Electron Transfer between CdS Nanorods and [FeFe] Hydrogenase and the Subsequent H 2 Generation journal December 2017
Nanowire–Bacteria Hybrids for Unassisted Solar Carbon Dioxide Fixation to Value-Added Chemicals journal April 2015
Cysteine–Cystine Photoregeneration for Oxygenic Photosynthesis of Acetic Acid from CO 2 by a Tandem Inorganic–Biological Hybrid System journal August 2016
Proton Reduction Using a Hydrogenase-Modified Nanoporous Black Silicon Photoelectrode journal June 2016
Photocatalytic Regeneration of Nicotinamide Cofactors by Quantum Dot–Enzyme Biohybrid Complexes journal February 2016
Light-Driven H 2 Evolution and C═C or C═O Bond Hydrogenation by Shewanella oneidensis : A Versatile Strategy for Photocatalysis by Nonphotosynthetic Microorganisms journal October 2017
Supramolecular Porphyrin Cages Assembled at Molecular–Materials Interfaces for Electrocatalytic CO Reduction journal September 2017
Solar-Driven Reduction of 1 atm of CO 2 to Formate at 10% Energy-Conversion Efficiency by Use of a TiO 2 -Protected III–V Tandem Photoanode in Conjunction with a Bipolar Membrane and a Pd/C Cathode journal September 2016
Nanoelectronic Investigation Reveals the Electrochemical Basis of Electrical Conductivity in Shewanella and Geobacter journal November 2016
Two Different Charge Separation Pathways in Photosystem II journal May 2010
Long-term Operation of Microbial Electrosynthesis Systems Improves Acetate Production by Autotrophic Microbiomes journal May 2013
Controlled Assembly of Hydrogenase-CdTe Nanocrystal Hybrids for Solar Hydrogen Production journal July 2010
Characterization of Photochemical Processes for H 2 Production by CdS Nanorod–[FeFe] Hydrogenase Complexes journal March 2012
Photoelectrochemical Water Oxidation with Photosystem II Integrated in a Mesoporous Indium–Tin Oxide Electrode journal May 2012
Direct Evidence of Active-Site Reduction and Photodriven Catalysis in Sensitized Hydrogenase Assemblies journal June 2012
Covalent Immobilization of Oriented Photosystem II on a Nanostructured Electrode for Solar Water Oxidation journal July 2013
Engineered Photosystem II Reaction Centers Optimize Photochemistry versus Photoprotection at Different Solar Intensities journal February 2014
Visible Light-Driven H 2 Production by Hydrogenases Attached to Dye-Sensitized TiO 2 Nanoparticles journal December 2009
Efficient and Clean Photoreduction of CO 2 to CO by Enzyme-Modified TiO 2 Nanoparticles Using Visible Light journal February 2010
Wiring of Photosystem II to Hydrogenase for Photoelectrochemical Water Splitting journal June 2015
Achieving Selective and Efficient Electrocatalytic Activity for CO 2 Reduction Using Immobilized Silver Nanoparticles journal October 2015
Mesostructure-Induced Selectivity in CO 2 Reduction Catalysis journal November 2015
Through-Space Charge Interaction Substituent Effects in Molecular Catalysis Leading to the Design of the Most Efficient Catalyst of CO 2 -to-CO Electrochemical Conversion journal December 2016
Carbon Dots as Versatile Photosensitizers for Solar-Driven Catalysis with Redox Enzymes journal December 2016
The In Vivo Potential-Regulated Protective Protein of Nitrogenase in Azotobacter vinelandii Supports Aerobic Bioelectrochemical Dinitrogen Reduction In Vitro journal June 2017
Photoelectrochemistry of Photosystem II in Vitro vs in Vivo journal October 2017
Physical Biology of the Materials–Microorganism Interface journal February 2018
Electroenzymatic C–C Bond Formation from CO 2 journal April 2018
Understanding Trends in the Electrocatalytic Activity of Metals and Enzymes for CO 2 Reduction to CO journal January 2013
Bacterial Recognition of Silicon Nanowire Arrays journal May 2013
Salt-Induced Self-Assembly of Bacteria on Nanowire Arrays journal August 2014
Comparison of Nonprecious Metal Cathode Materials for Methane Production by Electromethanogenesis journal February 2014
Solar energy conversion by chloroplast photoelectrochemical cells journal January 1981
Photoelectrochemical pumping of enzymatic CO2 reduction journal May 1984
Extracellular electron transfer via microbial nanowires journal June 2005
Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde journal November 2009
Hybrid bio-photo-electro-chemical cells for solar water splitting journal August 2016
Harnessing the power of microbial autotrophy journal September 2016
Microbial electrosynthesis — revisiting the electrical route for microbial production journal October 2010
Bias-free photoelectrochemical water splitting with photosystem II on a dye-sensitized photoanode wired to hydrogenase journal September 2018
The ins and outs of microorganism–electrode electron transfer reactions journal March 2017
Exploring the use of electrochemical impedance spectroscopy (EIS) in microbial fuel cell studies journal January 2009
Catalytic electrochemistry of a [NiFeSe]-hydrogenase on TiO2 and demonstration of its suitability for visible-light driven H 2 production journal January 2009
Photosynthetic production of ethanol from carbon dioxide in genetically engineered cyanobacteria journal January 2012
Improved cathode materials for microbial electrosynthesis journal January 2013
Photo-electrochemical communication between cyanobacteria (Leptolyngbia sp.) and osmium redox polymer modified electrodes journal January 2014
Protein film photoelectrochemistry of the water oxidation enzyme photosystem II journal January 2014
Biophotovoltaics: oxygenic photosynthetic organisms in the world of bioelectrochemical systems journal January 2015
Direct electron transfer from photosystem II to hematite in a hybrid photoelectrochemical cell journal January 2015
Experimental demonstrations of spontaneous, solar-driven photoelectrochemical water splitting journal January 2015
A monolithically integrated, intrinsically safe, 10% efficient, solar-driven water-splitting system based on active, stable earth-abundant electrocatalysts in conjunction with tandem III–V light absorbers protected by amorphous TiO 2 films journal January 2015
Co-assembly of photosystem II/reduced graphene oxide multilayered biohybrid films for enhanced photocurrent journal January 2015
Carbon nitride–TiO 2 hybrid modified with hydrogenase for visible light driven hydrogen production journal January 2015
Strategies for stable water splitting via protected photoelectrodes journal January 2017
Rational wiring of photosystem II to hierarchical indium tin oxide electrodes using redox polymers journal January 2016
Nitrogenase bioelectrocatalysis: heterogeneous ammonia and hydrogen production by MoFe protein journal January 2016
Balancing electron transfer rate and driving force for efficient photocatalytic hydrogen production in CdSe/CdS nanorod–[NiFe] hydrogenase assemblies journal January 2017
Many ways towards ‘solar fuel’: quantitative analysis of the most promising strategies and the main challenges during scale-up journal January 2018
Photoelectrocatalytic H 2 evolution in water with molecular catalysts immobilised on p-Si via a stabilising mesoporous TiO 2 interlayer journal January 2017
Pyrene hydrogel for promoting direct bioelectrochemistry: ATP-independent electroenzymatic reduction of N 2 journal January 2018
Microalgae as biodiesel & biomass feedstocks: Review & analysis of the biochemistry, energetics & economics journal January 2010
Water electrolysis and photoelectrolysis on electrodes engineered using biological and bio-inspired molecular systems journal January 2010
High photo-electrochemical activity of thylakoid–carbon nanotube composites for photosynthetic energy conversion journal January 2013
Electron transfer in proteins journal January 1995
Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: Pheophytin is the primary electron acceptor journal April 2006
Powering the planet: Chemical challenges in solar energy utilization journal October 2006
Probing electron transfer mechanisms in Shewanella oneidensis MR-1 using a nanoelectrode platform and single-cell imaging journal September 2010
Reversibility and efficiency in electrocatalytic energy conversion and lessons from enzymes journal August 2011
Shewanella oneidensis MR-1 nanowires are outer membrane and periplasmic extensions of the extracellular electron transport components journal August 2014
Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system journal February 2015
Hybrid bioinorganic approach to solar-to-chemical conversion journal August 2015
Spectroscopic elucidation of energy transfer in hybrid inorganic–biological organisms for solar-to-chemical production journal October 2016
Ambient nitrogen reduction cycle using a hybrid inorganic–biological system journal June 2017
Multi-haem cytochromes in Shewanella oneidensis MR-1: structures, functions and opportunities journal January 2015
Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement journal May 2011
Ionic Liquid-Mediated Selective Conversion of CO2 to CO at Low Overpotentials journal September 2011
High-Performance Silicon Photoanodes Passivated with Ultrathin Nickel Films for Water Oxidation journal November 2013
Amorphous TiO2 coatings stabilize Si, GaAs, and GaP photoanodes for efficient water oxidation journal May 2014
A Monolithic Photovoltaic-Photoelectrochemical Device for Hydrogen Production via Water Splitting journal April 1998
Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production journal December 2015
Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid journal April 2016
Water splitting–biosynthetic system with CO 2 reduction efficiencies exceeding photosynthesis journal June 2016
Aerobic Hydrogen Production via Nitrogenase in Azotobacter vinelandii CA6 journal April 2015
Redirecting Reductant Flux into Hydrogen Production via Metabolic Engineering of Fermentative Carbon Metabolism in a Cyanobacterium journal June 2010
Improving Photosynthetic Efficiency for Greater Yield journal June 2010
Electron Transfer in Proteins journal June 1996
Electrochemical Gating of Tricarboxylic Acid Cycle in Electricity-Producing Bacterial Cells of Shewanella journal August 2013
Rational wiring of photosystem II to hierarchical indium tin oxide electrodes using redox polymers text January 2016
Photoelectrochemistry of Photosystem II in Vitro vs in Vivo. journalarticle January 2018
Solar Water Splitting with a Hydrogenase Integrated in Photoelectrochemical Tandem Cells. journalarticle January 2018
Photoelectrochemical H2 Evolution with a Hydrogenase Immobilized on a TiO2-Protected Silicon Electrode. journalarticle January 2016
Solar Water Splitting with a Hydrogenase Integrated in Photoelectrochemical Tandem Cells text January 2018
Carbon Dots as Versatile Photosensitizers for Solar-Driven Catalysis with Redox Enzymes text January 2016

Cited By (35)

Interfacing Formate Dehydrogenase with Metal Oxides for the Reversible Electrocatalysis and Solar‐Driven Reduction of Carbon Dioxide journal February 2019
Examination of abiotic cofactor assembly in photosynthetic biomimetics: site-specific stereoselectivity in the conjugation of a ruthenium(II) tris(bipyridine) photosensitizer to a multi-heme protein journal January 2020
Advancing Techniques for Investigating the Enzyme–Electrode Interface journal May 2019
Integration of a Hydrogenase in a Lead Halide Perovskite Photoelectrode for Tandem Solar Water Splitting journal December 2019
Water oxidation by Ferritin: A semi-natural electrode journal August 2019
A three-dimensional hybrid electrode with electroactive microbes for efficient electrogenesis and chemical synthesis journal February 2020
Nanobiohybrids: Materials approaches for bioaugmentation journal March 2020
Semiconductor Quantum Dots: An Emerging Candidate for CO 2 Photoreduction journal June 2019
Catalysis of a Single Transition Metal Site for Water Oxidation: From Mononuclear Molecules to Single Atoms journal December 2019
Solar Heat‐Enhanced Energy Conversion in Devices Based on Photosynthetic Membranes and PEDOT:PSS‐Nanocellulose Electrodes journal December 2019
Hybrid Photoelectrochemical Water Splitting Systems: From Interface Design to System Assembly journal June 2019
Optical Shading Induces an In‐Plane Potential Gradient in a Semiartificial Photosynthetic System Bringing Photoelectric Synergy journal August 2019
Interfacing Formate Dehydrogenase with Metal Oxides for the Reversible Electrocatalysis and Solar‐Driven Reduction of Carbon Dioxide journal February 2019
Surface‐Polarity‐Induced Spatial Charge Separation Boosts Photocatalytic Overall Water Splitting on GaN Nanorod Arrays journal November 2019
Interfacing Formate Dehydrogenase with Metal Oxides for the Reversible Electrocatalysis and Solar‐Driven Reduction of Carbon Dioxide journal February 2019
Surface‐Polarity‐Induced Spatial Charge Separation Boosts Photocatalytic Overall Water Splitting on GaN Nanorod Arrays journal January 2020
Cascade‐Amplified Time‐Resolved Fluorescent Assay Driven by an Enzyme‐Integrated Catalytic Compartment as an Artificial Multi‐Enzyme Complex journal June 2019
Mononuclear Ru(II) PolyPyridyl Water Oxidation Catalysts Decorated with Perfluoroalkyl C 8 H 17 -Tag Bearing Chains : Mononuclear Ru(II) PolyPyridyl Water Oxidation Catalysts Decorated with Perfluoroalkyl C journal October 2019
Coupling biology to synthetic nanomaterials for semi-artificial photosynthesis journal October 2019
Examination of abiotic cofactor assembly in photosynthetic biomimetics: site-specific stereoselectivity in the conjugation of a ruthenium(II) tris(bipyridine) photosensitizer to a multi-heme protein journal January 2020
Photosynthetic apparatus of Rhodobacter sphaeroides exhibits prolonged charge storage journal February 2019
Advancing photosystem II photoelectrochemistry for semi-artificial photosynthesis journal December 2019
Perfluorocarbon nanoemulsion promotes the delivery of reducing equivalents for electricity-driven microbial CO2 reduction journal April 2019
Bioelectrocatalysis as the basis for the design of enzyme-based biofuel cells and semi-artificial biophotoelectrodes journal November 2019
Artificial photosynthesis: opportunities and challenges of molecular catalysts journal January 2019
Advanced space- and time-resolved techniques for photocatalyst studies journal January 2020
A thiophene-modified doubleshell hollow g-C 3 N 4 nanosphere boosts NADH regeneration via synergistic enhancement of charge excitation and separation journal January 2019
A photosystem I monolayer with anisotropic electron flow enables Z-scheme like photosynthetic water splitting journal January 2019
Enhanced CO 2 reduction and valuable C 2+ chemical production by a CdS-photosynthetic hybrid system journal January 2019
Light-driven carbon−carbon bond formation via CO 2 reduction catalyzed by complexes of CdS nanorods and a 2-oxoacid oxidoreductase journal December 2019
Quantum dot interactions with and toxicity to Shewanella oneidensis MR-1 journal January 2020
Immobilization of functional nano-objects in living engineered bacterial biofilms for catalytic applications journal July 2019
Interfacing Formate Dehydrogenase with Metal Oxides for the Reversible Electrocatalysis and Solar‐Driven Reduction of Carbon Dioxide text January 2019
Interfacing Formate Dehydrogenase with Metal Oxides for the Reversible Electrocatalysis and Solar-Driven Reduction of Carbon Dioxide text January 2019
Green Synthetic Fuels: Renewable Routes for the Conversion of Non-Fossil Feedstocks into Gaseous Fuels and Their End Uses journal January 2020

Similar Records

Coupling biology to synthetic nanomaterials for semi-artificial photosynthesis
Journal Article · 2019 · Photosynthesis Research · OSTI ID:1573197

Chemical approaches to artificial photosynthesis
Journal Article · 1989 · Accounts of Chemical Research; (USA) · OSTI ID:7155513

Carbon dioxide fixation by artificial photosynthesis
Conference · 1993 · OSTI ID:249747