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Title: Spectroscopic elucidation of energy transfer in hybrid inorganic–biological organisms for solar-to-chemical production

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [1];  [1];  [1];  [2];  [1];  [3];  [2]
  1. Univ. of California, Berkeley, CA (United States). Department of Chemistry
  2. Univ. of California, Berkeley, CA (United States). Department of Chemistry and Department of Materials Science and Engineering; Kavli Energy NanoSciences Institute, Berkeley, CA (United States)
  3. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Foundry
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We present that the rise of inorganic–biological hybrid organisms for solar-to-chemical production has spurred mechanistic investigations into the dynamics of the biotic–abiotic interface to drive the development of next-generation systems. The model system, Moorella thermoacetica–cadmium sulfide (CdS), combines an inorganic semiconductor nanoparticle light harvester with an acetogenic bacterium to drive the photosynthetic reduction of CO2 to acetic acid with high efficiency. In this work, we report insights into this unique electrotrophic behavior and propose a charge-transfer mechanism from CdS to M. thermoacetica. Transient absorption (TA) spectroscopy revealed that photoexcited electron transfer rates increase with increasing hydrogenase (H2ase) enzyme activity. On the same time scale as the TA spectroscopy, time-resolved infrared (TRIR) spectroscopy showed spectral changes in the 1,700–1,900-cm-1 spectral region. The quantum efficiency of this system for photosynthetic acetic acid generation also increased with increasing H2ase activity and shorter carrier lifetimes when averaged over the first 24 h of photosynthesis. However, within the initial 3 h of photosynthesis, the rate followed an opposite trend: The bacteria with the lowest H2ase activity photosynthesized acetic acid the fastest. These results suggest a two-pathway mechanism: a high quantum efficiency charge-transfer pathway to H2ase generating H2 as a molecular intermediate that dominates at long time scales (24 h), and a direct energy-transducing enzymatic pathway responsible for acetic acid production at short time scales (3 h). Lastly, this work represents a promising platform to utilize conventional spectroscopic methodology to extract insights from more complex biotic–abiotic hybrid systems.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)
Grant/Contract Number:
AC02-05CH11231; DMR-1507914
OSTI ID:
1377542
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, Issue 42; ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)Copyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 98 works
Citation information provided by
Web of Science

References (42)

Probing intermediates in the activation cycle of [NiFe] hydrogenase by infrared spectroscopy: the Ni-SIr state and its light sensitivity journal July 2009
Quantitative IR spectrophotometry of peptide compounds in water (H2O) solutions. I. Spectral parameters of amino acid residue absorption bands journal January 1990
Fourier Transform Infrared Spectroscopic Analysis of Protein Secondary Structures journal August 2007
Autotrophy at the thermodynamic limit of life: a model for energy conservation in acetogenic bacteria journal November 2014
Demonstration of hydrogenase in extracts of the homoacetate-fermenting bacterium Clostridium thermoaceticum. journal January 1982
Optimal metal domain size for photocatalysis with hybrid semiconductor-metal nanorods journal January 2016
Nanowire–Bacteria Hybrids for Unassisted Solar Carbon Dioxide Fixation to Value-Added Chemicals journal April 2015
Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production journal December 2015
Limitations and prospects of natural photosynthesis for bioenergy production journal June 2010
Energy and environment policy case for a global project on artificial photosynthesis journal January 2013
Organelle-Targetable Fluorescent Probes for Imaging Hydrogen Peroxide in Living Cells via SNAP-Tag Protein Labeling journal March 2010
Characterization of the H2- and CO-dependent chemolithotrophic potentials of the acetogens Clostridium thermoaceticum and Acetogenium kivui. journal August 1990
Designing interfaces of hydrogenase–nanomaterial hybrids for efficient solar conversion journal August 2013
Electron transfer in proteins journal January 1995
Enzyme mechanism as a kinetic control element for designing synthetic biofuel pathways journal February 2011
Hybrid bioinorganic approach to solar-to-chemical conversion journal August 2015
Inulinase Immobilized Lectin Affinity Magnetic Nanoparticles for Inulin Hydrolysis journal January 2021
Competition between electron transfer, trapping, and recombination in CdS nanorod–hydrogenase complexes journal January 2015
Microbial electron transport and energy conservation – the foundation for optimizing bioelectrochemical systems journal June 2015
Unraveling the Structure and Dynamics of Excitons in Semiconductor Quantum Dots journal January 2011
Electrochemical insights into the mechanism of NiFe membrane-bound hydrogenases journal February 2016
Redesigning photosynthesis to sustainably meet global food and bioenergy demand journal June 2015
The complete genome sequence of Moorella thermoacetica (f. Clostridium thermoaceticum) journal July 2008
Activation and Inactivation of Hydrogenase Function and the Catalytic Cycle: Spectroelectrochemical Studies journal December 2007
Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement journal May 2011
An in situ surface electrochemistry approach towards whole-cell studies: the structure and reactivity of a Geobacter sulfurreducens submonolayer on electrified metal/electrolyte interfaces journal January 2014
Long-range electron transfer journal February 2005
Cathodes as electron donors for microbial metabolism: Which extracellular electron transfer mechanisms are involved? journal January 2011
Photoinduced electron transfer from colloidal cadmium sulfide to methylviologen: a picosecond transient absorption study journal January 1988
Carbon Monoxide and Cyanide as Intrinsic Ligands to Iron in the Active Site of [NiFe]-Hydrogenases: NiFe(CN) journal February 1999
Activation and Inactivation of Hydrogenase Function and the Catalytic Cycle:  Spectroelectrochemical Studies journal October 2007
Mutations to R. sphaeroides Reaction Center Perturb Energy Levels and Vibronic Coupling but Not Observed Energy Transfer Rates journal December 2015
Electron Transfer Kinetics in CdS Nanorod–[FeFe]-Hydrogenase Complexes and Implications for Photochemical H 2 Generation journal March 2014
Electron Transfer in Proteins journal June 1996
Artificial Photosynthesis for Sustainable Fuel and Chemical Production journal January 2015
Chemistry of the Triplet 14-Electron Complex Fe(CO) 3 in Solution Studied by Ultrafast Time-Resolved IR Spectroscopy journal May 2012
Direct electrochemistry of an [FeFe]-hydrogenase on a TiO2 Electrode journal January 2011
Direct Evidence of Active-Site Reduction and Photodriven Catalysis in Sensitized Hydrogenase Assemblies journal June 2012
Charge Transfer Dynamics between Photoexcited CdS Nanorods and Mononuclear Ru Water-Oxidation Catalysts journal February 2013
An in situ surface electrochemistry approach towards whole-cell studies: the structure and reactivity of a Geobacter sulfurreducens submonolayer on electrified metal/electrolyte interfaces text January 2014
Efficient solar-to-fuels production from a hybrid microbial–water-splitting catalyst system journal February 2015
Frontiers, Opportunities, and Challenges in Biochemical and Chemical Catalysis of CO 2 Fixation journal June 2013

Cited By (13)

Engineering microbial consortia by division of labor journal February 2019
Interfacing nature's catalytic machinery with synthetic materials for semi-artificial photosynthesis. text January 2018
Stimulating bioplastic production with light energy by coupling Ralstonia eutropha with the photocatalyst graphitic carbon nitride journal January 2019
Metallic Cobalt-Carbon Composite as Recyclable and Robust Magnetic Photocatalyst for Efficient CO 2 Reduction journal July 2018
Review on optofluidic microreactors for artificial photosynthesis journal January 2018
Combinatorial design of chemical‐dependent protein switches for controlling intracellular electron transfer journal September 2019
Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production journal October 2018
Extracellular electron transfer in acetogenic bacteria and its application for conversion of carbon dioxide into organic compounds journal July 2017
Solar-energy-facilitated CdS x Se 1−x quantum dot bio-assembly in Escherichia coli and Tetrahymena pyriformis journal January 2019
Light-driven fine chemical production in yeast biohybrids journal November 2018
Optically responsive delivery platforms: from the design considerations to biomedical applications journal January 2020
Interfacing nature’s catalytic machinery with synthetic materials for semi-artificial photosynthesis journal October 2018
Solar-driven carbon dioxide fixation using photosynthetic semiconductor bio-hybrids journal January 2019

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Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
14 SOLAR ENERGY
30 DIRECT ENERGY CONVERSION
energy conversion
spectroscopy
CO2 reduction
biohybrid systems
catalysis