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Title: Interprotein electron transfer biohybrid system for photocatalytic H2 production

Abstract

Around the world there is a large research investment in developing solar fuel systems as clean and sustainable sources of energy. The fundamental mechanisms of natural photosynthesis can provide a source of inspiration for these studies. Photosynthetic reaction center (RC) proteins capture and convert light energy into chemical energy that is ultimately used to drive oxygenic water-splitting and carbon fixation. For the light energy to be used, the RC communicates with other donor/acceptor components via a sophisticated electron transfer scheme that includes electron transfer reactions between soluble and membrane bound proteins. Herein, we reengineer an inherent interprotein electron transfer pathway in a natural photosynthetic system to make it photocatalytic for aqueous H2 production. The native electron shuttle protein ferredoxin (Fd) is used as a scaffold for binding of a ruthenium photosensitizer and H2 catalytic function is imparted to its partner protein, ferredoxin-NADP+-reductase (FNR), by attachment of cobaloxime molecules. We find that this 2-protein biohybrid system produces H2 in aqueous solutions via light-induced interprotein electron transfer reactions (TON > 2500 H2/FNR), providing insight about using native protein-protein interactions as a method for fuel generation.

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1]
  1. Argonne National Lab. (ANL), Argonne, IL (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division
OSTI Identifier:
1606243
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Photosynthesis Research
Additional Journal Information:
Journal Volume: 143; Journal Issue: 2; Journal ID: ISSN 0166-8595
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biohybrid; ferredoxin; ferredoxin-NADP+-reductase; photosynthetic electron transfer; solar fuel; solar hydrogen production

Citation Formats

Brahmachari, Udita, Pokkuluri, P. Raj, Tiede, David M., Niklas, Jens, Poluektov, Oleg G., Mulfort, Karen L., and Utschig, Lisa M. Interprotein electron transfer biohybrid system for photocatalytic H2 production. United States: N. p., 2020. Web. doi:10.1007/s11120-019-00705-x.
Brahmachari, Udita, Pokkuluri, P. Raj, Tiede, David M., Niklas, Jens, Poluektov, Oleg G., Mulfort, Karen L., & Utschig, Lisa M. Interprotein electron transfer biohybrid system for photocatalytic H2 production. United States. doi:10.1007/s11120-019-00705-x.
Brahmachari, Udita, Pokkuluri, P. Raj, Tiede, David M., Niklas, Jens, Poluektov, Oleg G., Mulfort, Karen L., and Utschig, Lisa M. Fri . "Interprotein electron transfer biohybrid system for photocatalytic H2 production". United States. doi:10.1007/s11120-019-00705-x.
@article{osti_1606243,
title = {Interprotein electron transfer biohybrid system for photocatalytic H2 production},
author = {Brahmachari, Udita and Pokkuluri, P. Raj and Tiede, David M. and Niklas, Jens and Poluektov, Oleg G. and Mulfort, Karen L. and Utschig, Lisa M.},
abstractNote = {Around the world there is a large research investment in developing solar fuel systems as clean and sustainable sources of energy. The fundamental mechanisms of natural photosynthesis can provide a source of inspiration for these studies. Photosynthetic reaction center (RC) proteins capture and convert light energy into chemical energy that is ultimately used to drive oxygenic water-splitting and carbon fixation. For the light energy to be used, the RC communicates with other donor/acceptor components via a sophisticated electron transfer scheme that includes electron transfer reactions between soluble and membrane bound proteins. Herein, we reengineer an inherent interprotein electron transfer pathway in a natural photosynthetic system to make it photocatalytic for aqueous H2 production. The native electron shuttle protein ferredoxin (Fd) is used as a scaffold for binding of a ruthenium photosensitizer and H2 catalytic function is imparted to its partner protein, ferredoxin-NADP+-reductase (FNR), by attachment of cobaloxime molecules. We find that this 2-protein biohybrid system produces H2 in aqueous solutions via light-induced interprotein electron transfer reactions (TON > 2500 H2/FNR), providing insight about using native protein-protein interactions as a method for fuel generation.},
doi = {10.1007/s11120-019-00705-x},
journal = {Photosynthesis Research},
number = 2,
volume = 143,
place = {United States},
year = {2020},
month = {1}
}

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Works referenced in this record:

Ru–protein–Co biohybrids designed for solar hydrogen production: understanding electron transfer pathways related to photocatalytic function
journal, January 2016

  • Soltau, Sarah R.; Dahlberg, Peter D.; Niklas, Jens
  • Chemical Science, Vol. 7, Issue 12
  • DOI: 10.1039/C6SC03121H

Photocatalytic Hydrogen Production from Noncovalent Biohybrid Photosystem I/Pt Nanoparticle Complexes
journal, January 2011

  • Utschig, Lisa M.; Dimitrijevic, Nada M.; Poluektov, Oleg G.
  • The Journal of Physical Chemistry Letters, Vol. 2, Issue 3
  • DOI: 10.1021/jz101728v

Analysis of the Oxidation-Reduction Potentials of Recombinant Ferredoxin-NADP+ Reductase from Spinach Chloroplasts
journal, August 1996


Molecular Cobalt Catalysts for H 2 Generation with Redox Activity and Proton Relays in the Second Coordination Sphere
journal, December 2018


Light-driven hydrogen production from Photosystem I-catalyst hybrids
journal, April 2015

  • Utschig, Lisa M.; Soltau, Sarah R.; Tiede, David M.
  • Current Opinion in Chemical Biology, Vol. 25
  • DOI: 10.1016/j.cbpa.2014.11.019

Synechocystis ferredoxin/ferredoxin-NADP + -reductase/NADP + complex: Structural model obtained by NMR-restrained docking
journal, August 2005


Unimolecular and bimolecular homolytic reactions of organochromium and organocobalt complexes. Kinetics and equilibria
journal, September 1984

  • Bakac, Andreja; Espenson, James H.
  • Journal of the American Chemical Society, Vol. 106, Issue 18
  • DOI: 10.1021/ja00330a027

Powering the planet: Chemical challenges in solar energy utilization
journal, October 2006

  • Lewis, N. S.; Nocera, D. G.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 43, p. 15729-15735
  • DOI: 10.1073/pnas.0603395103

Charge Separation Related to Photocatalytic H 2 Production from a Ru–Apoflavodoxin–Ni Biohybrid
journal, December 2016


Nature-Driven Photochemistry for Catalytic Solar Hydrogen Production: A Photosystem I–Transition Metal Catalyst Hybrid
journal, October 2011

  • Utschig, Lisa M.; Silver, Sunshine C.; Mulfort, Karen L.
  • Journal of the American Chemical Society, Vol. 133, Issue 41
  • DOI: 10.1021/ja206012r

The Hydrogen Catalyst Cobaloxime: A Multifrequency EPR and DFT Study of Cobaloxime’s Electronic Structure
journal, February 2012

  • Niklas, Jens; Mardis, Kristy L.; Rakhimov, Rakhim R.
  • The Journal of Physical Chemistry B, Vol. 116, Issue 9
  • DOI: 10.1021/jp209395n

Role of critical charged residues in reduction potential modulation of ferredoxin-NADP + reductase: Differential stabilization of FAD redox forms
journal, May 2002


Crystallographic studies of the interaction between the ferredoxin-NADP + reductase and ferredoxin from the cyanobacterium Anabaena : looking for the elusive ferredoxin molecule
journal, November 2000

  • Morales, Renaud; Kachalova, Galina; Vellieux, Frédéric
  • Acta Crystallographica Section D Biological Crystallography, Vol. 56, Issue 11
  • DOI: 10.1107/S0907444900010052

Wiring Photosystem I for Direct Solar Hydrogen Production
journal, January 2010

  • Lubner, Carolyn E.; Grimme, Rebecca; Bryant, Donald A.
  • Biochemistry, Vol. 49, Issue 3
  • DOI: 10.1021/bi901704v

Probing Local Dynamics of the Photosynthetic Bacterial Reaction Center with a Cysteine Specific Spin Label
journal, June 2003

  • Poluektov, Oleg G.; Utschig, Lisa M.; Dalosto, Sergio
  • The Journal of Physical Chemistry B, Vol. 107, Issue 25
  • DOI: 10.1021/jp0342374

Mechanism of Coenzyme Recognition and Binding Revealed by Crystal Structure Analysis of Ferredoxin–NADP+ Reductase Complexed with NADP+
journal, June 2002


Efficient and Clean Photoreduction of CO 2 to CO by Enzyme-Modified TiO 2 Nanoparticles Using Visible Light
journal, February 2010

  • Woolerton, Thomas W.; Sheard, Sally; Reisner, Erwin
  • Journal of the American Chemical Society, Vol. 132, Issue 7
  • DOI: 10.1021/ja910091z

Toward Cost-Effective Solar Energy Use
journal, February 2007


Aqueous light driven hydrogen production by a Ru–ferredoxin–Co biohybrid
journal, January 2015

  • Soltau, S. R.; Niklas, J.; Dahlberg, P. D.
  • Chemical Communications, Vol. 51, Issue 53
  • DOI: 10.1039/C5CC03006D

Characterization of the structure, properties, and reactivity of a cobalt(II) macrocyclic complex
journal, November 1986

  • Bakac, Andreja; Brynildson, Mark E.; Espenson, James H.
  • Inorganic Chemistry, Vol. 25, Issue 23
  • DOI: 10.1021/ic00243a012

Structure of the Mutant E92K of [2Fe–2S] Ferredoxin I from Spinacia oleracea at 1.7 Å Resolution
journal, November 1998

  • Binda, Claudia; Coda, Alessandro; Aliverti, Alessandro
  • Acta Crystallographica Section D Biological Crystallography, Vol. 54, Issue 6
  • DOI: 10.1107/S0907444998005137

Solar hydrogen-producing bionanodevice outperforms natural photosynthesis
journal, December 2011

  • Lubner, C. E.; Applegate, A. M.; Knorzer, P.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 52
  • DOI: 10.1073/pnas.1114660108

Modular Homogeneous Chromophore–Catalyst Assemblies
journal, April 2016


Role of Arg100 and Arg264 from Anabaena PCC 7119 Ferredoxin−NADP + Reductase for Optimal NADP + Binding and Electron Transfer
journal, December 1998

  • Martínez-Júlvez, Marta; Hermoso, Juan; Hurley, John K.
  • Biochemistry, Vol. 37, Issue 51
  • DOI: 10.1021/bi981718i

Z-scheme solar water splitting via self-assembly of photosystem I-catalyst hybrids in thylakoid membranes
journal, January 2018

  • Utschig, Lisa M.; Soltau, Sarah R.; Mulfort, Karen L.
  • Chemical Science, Vol. 9, Issue 45
  • DOI: 10.1039/C8SC02841A

Interfacing Formate Dehydrogenase with Metal Oxides for the Reversible Electrocatalysis and Solar‐Driven Reduction of Carbon Dioxide
journal, February 2019

  • Miller, Melanie; Robinson, William E.; Oliveira, Ana Rita
  • Angewandte Chemie, Vol. 131, Issue 14
  • DOI: 10.1002/ange.201814419

Binuclear Ruthenium−Manganese Complexes as Simple Artificial Models for Photosystem II in Green Plants
journal, July 1997

  • Sun, Licheng; Berglund, Helena; Davydov, Roman
  • Journal of the American Chemical Society, Vol. 119, Issue 30
  • DOI: 10.1021/ja962511k

Protein Delivery of a Ni Catalyst to Photosystem I for Light-Driven Hydrogen Production
journal, August 2013

  • Silver, Sunshine C.; Niklas, Jens; Du, Pingwu
  • Journal of the American Chemical Society, Vol. 135, Issue 36
  • DOI: 10.1021/ja405277g

EasySpin, a comprehensive software package for spectral simulation and analysis in EPR
journal, January 2006


Chemical Approaches to Artificial Photosynthesis. 2
journal, October 2005

  • Alstrum-Acevedo, James H.; Brennaman, M. Kyle; Meyer, Thomas J.
  • Inorganic Chemistry, Vol. 44, Issue 20
  • DOI: 10.1021/ic050904r

Light-driven dinitrogen reduction catalyzed by a CdS:nitrogenase MoFe protein biohybrid
journal, April 2016


Influence of pH and ionic strength on electrostatic properties of ferredoxin, FNR, and hydrogenase and the rate constants of their interaction
journal, October 2016


Association of Ferredoxin:NADP+ oxidoreductase with the photosynthetic apparatus modulates electron transfer in Chlamydomonas reinhardtii
journal, June 2017


Formation of thin polymeric films by electropolymerization. Reduction of metal complexes containing bromomethyl-substituted derivatives of 2,2'-bipyridine
journal, July 1991

  • Gould, Sharon.; Strouse, Geoffrey F.; Meyer, Thomas J.
  • Inorganic Chemistry, Vol. 30, Issue 14
  • DOI: 10.1021/ic00014a022

Light-driven Hydrogen Production by a Hybrid Complex of a [NiFe]-Hydrogenase and the Cyanobacterial Photosystem I
journal, January 2006

  • Ihara, Masaki; Nishihara, Hirofumi; Yoon, Ki-Seok
  • Photochemistry and Photobiology, Vol. 82, Issue 3
  • DOI: 10.1562/2006-01-16-RA-778

Self-organized photosynthetic nanoparticle for cell-free hydrogen production
journal, November 2009

  • Iwuchukwu, Ifeyinwa J.; Vaughn, Michael; Myers, Natalie
  • Nature Nanotechnology, Vol. 5, Issue 1
  • DOI: 10.1038/nnano.2009.315

Photosystem I/Molecular Wire/Metal Nanoparticle Bioconjugates for the Photocatalytic Production of H 2
journal, May 2008

  • Grimme, Rebecca A.; Lubner, Carolyn E.; Bryant, Donald A.
  • Journal of the American Chemical Society, Vol. 130, Issue 20
  • DOI: 10.1021/ja800923y

Rational redesign of the ferredoxin-NADP+-oxido-reductase/ferredoxin-interaction for photosynthesis-dependent H2-production
journal, April 2018

  • Wiegand, K.; Winkler, M.; Rumpel, S.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1859, Issue 4
  • DOI: 10.1016/j.bbabio.2018.01.006

Structure–function relationships in Anabaena ferredoxin/ferredoxin:NADP+ reductase electron transfer: insights from site-directed mutagenesis, transient absorption spectroscopy and X-ray crystallography
journal, April 2002

  • Hurley, John K.; Morales, Renaud; Martı́nez-Júlvez, Marta
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1554, Issue 1-2
  • DOI: 10.1016/S0005-2728(02)00188-3