Cooperative Electronic and Structural Regulation in a Bioinspired Allosteric Photoredox Catalyst

Lifschitz, Alejo M.; Young, Ryan M.; Mendez-Arroyo, Jose; McGuirk, C. Michael; Wasielewski, Michael R.; Mirkin, Chad A.

doi:10.1021/acs.inorgchem.6b00095

Cooperative Electronic and Structural Regulation in a Bioinspired Allosteric Photoredox Catalyst

Journal Article · Tue May 10 00:00:00 EDT 2016 · Inorganic Chemistry

DOI:https://doi.org/10.1021/acs.inorgchem.6b00095· OSTI ID:1388175

Lifschitz, Alejo M. ^[1]; Young, Ryan M. ^[2]; Mendez-Arroyo, Jose ^[1]; McGuirk, C. Michael ^[1]; Wasielewski, Michael R. ^[2]; Mirkin, Chad A. ^[2]

Northwestern Univ., Evanston, IL (United States). International Inst. for Nanotechnology
Northwestern Univ., Evanston, IL (United States). International Inst. for Nanotechnology and Argonne-Northwestern Solar Energy Research (ANSER) Center

Here in this article, we report the first allosteric photoredox catalyst regulated via constructively coupled structural and electronic control. While often synergistically exploited in nature, these two types of control mechanisms have only been applied independently in the vast majority of allosteric enzyme mimics and receptors in the literature. By embedding a model of photosystem II in a supramolecular coordination complex that responds to chloride as an allosteric effector, we show that distance and electronic control of light harvesting can be married to maximize allosteric regulation of catalytic activity. This biomimetic system is composed of a Bodipy photoantenna, which is capable of transferring excited-state energy to a photoredox pair, wherein the excitation energy is used to generate a catalytically active charge-separated state. The structural aspect of allosteric regulation is achieved by toggling the coordination chemistry of an antenna-functionalized hemilabile ligand via partial displacement from a Rh^I structual node using chloride. In doing so, the distance between the antenna and the central photoredox catalyst is increased, lowering the inherent efficiency of through-space energy transfer. At the same time, coordination of chloride lowers both the charge of the Rh^I node and the reduction potential of the Rh^II/I couple, to the extent that electronic quenching of the antenna excited state is possible via photoinduced electron transfer from the metal center. Compared to a previously developed system that operates solely via electronic regulation, the present system demonstrates that coupling electronic and structural approaches to allosteric regulation gives rise to improved switching ratios between catalytically active and inactive states. Contributions from both structural and electronic control mechanisms are probed via nuclear magnetic resonance, X-ray diffraction, electrochemical, spectroelectrochemical, and transient absorption studies. Overall, this work establishes that intertwined electronic and structural regulatory mechanisms can be borrowed from nature to build stimuli-responsive inorganic materials with potential applications in sensing, catalysis, and photonic devices.

View Accepted Manuscript (DOE)

Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Argonne-Northwestern Solar Energy Research Center (ANSER)

Sponsoring Organization:: National Science Foundation (NSF); U.S. Army; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0001059

OSTI ID:: 1388175

Journal Information:: Inorganic Chemistry, Journal Name: Inorganic Chemistry Journal Issue: 17 Vol. 55; ISSN 0020-1669

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (29)

Enzyme Mimics Based Upon Supramolecular Coordination Chemistry Wiester, Michael J.; Ulmann, Pirmin A.; Mirkin, Chad A. Angewandte Chemie International Edition, Vol. 50, Issue 1 https://doi.org/10.1002/anie.201000380	journal	October 2010
FRET Studies on a Series of BODIPY‐Dye‐Labeled Switchable Resorcin[4]arene Cavitands Pochorovski, Igor; Breiten, Benjamin; Schweizer, W. Bernd Chemistry – A European Journal, Vol. 16, Issue 42 https://doi.org/10.1002/chem.201001625	journal	September 2010
Artificial Allosteric Receptors Kremer, Christopher; Lützen, Arne Chemistry - A European Journal, Vol. 19, Issue 20 https://doi.org/10.1002/chem.201203814	journal	March 2013
Beyond Stereoselectivity, Switchable Catalysis: Some of the Last Frontier Challenges in Ring-Opening Polymerization of Cyclic Esters Guillaume, Sophie M.; Kirillov, Evgueni; Sarazin, Yann Chemistry - A European Journal, Vol. 21, Issue 22 https://doi.org/10.1002/chem.201500613	journal	April 2015
Photosynthetic Antenna-Reaction Center Mimicry by Using Boron Dipyrromethene Sensitizers El-Khouly, Mohamed E.; Fukuzumi, Shunichi; D'Souza, Francis ChemPhysChem, Vol. 15, Issue 1 https://doi.org/10.1002/cphc.201300715	journal	November 2013
Artificial Light‐Harvesting Systems by Use of Metal Coordination Kobuke, Yoshiaki European Journal of Inorganic Chemistry, Vol. 2006, Issue 12 https://doi.org/10.1002/ejic.200600161	journal	May 2006
Redox potential, ligand and structural effects in rhodium(I) complexes Guedes da Silva, M. Fátima C.; Trzeciak, Anna M.; Ziólkowski, Józef J. Journal of Organometallic Chemistry, Vol. 620, Issue 1-2 https://doi.org/10.1016/S0022-328X(00)00816-0	journal	February 2001
Allosteric Supramolecular Receptors and Catalysts Kovbasyuk, Larisa; Krämer, Roland Chemical Reviews, Vol. 104, Issue 6 https://doi.org/10.1021/cr030673a	journal	June 2004
BODIPY Dyes and Their Derivatives: Syntheses and Spectroscopic Properties Loudet, Aurore; Burgess, Kevin Chemical Reviews, Vol. 107, Issue 11 https://doi.org/10.1021/cr078381n	journal	November 2007
Elucidating the Mechanism of the Halide-Induced Ligand Rearrangement Reaction Yoo, Hyojong; Rosen, Mari S.; Brown, Aaron M. Inorganic Chemistry, Vol. 51, Issue 21 https://doi.org/10.1021/ic3018776	journal	October 2012
Boron-Dipyrromethene-Functionalized Hemilabile Ligands as “Turn-On” Fluorescent Probes for Coordination Changes in Weak-Link Approach Complexes Lifschitz, Alejo M.; Shade, Chad M.; Spokoyny, Alexander M. Inorganic Chemistry, Vol. 52, Issue 9 https://doi.org/10.1021/ic400383t	journal	April 2013
Photonic Switching of Photoinduced Electron Transfer in a Dithienylethene−Porphyrin−Fullerene Triad Molecule Liddell, Paul A.; Kodis, Gerdenis; Moore, Ana L. Journal of the American Chemical Society, Vol. 124, Issue 26 https://doi.org/10.1021/ja026327c	journal	July 2002
Energy Transfer Followed by Electron Transfer in a Supramolecular Triad Composed of Boron Dipyrrin, Zinc Porphyrin, and Fullerene: A Model for the Photosynthetic Antenna-Reaction Center Complex D'Souza, Francis; Smith, Phillip M.; Zandler, Melvin E. Journal of the American Chemical Society, Vol. 126, Issue 25 https://doi.org/10.1021/ja030647u	journal	June 2004
Allosterically Regulated Supramolecular Catalysis of Acyl Transfer Reactions for Signal Amplification and Detection of Small Molecules Masar, Martin S.; Gianneschi, Nathan C.; Oliveri, Christopher G. Journal of the American Chemical Society, Vol. 129, Issue 33 https://doi.org/10.1021/ja0711516	journal	August 2007
Mimicking the Role of the Antenna in Photosynthetic Photoprotection Terazono, Yuichi; Kodis, Gerdenis; Bhushan, Kul Journal of the American Chemical Society, Vol. 133, Issue 9 https://doi.org/10.1021/ja107753f	journal	March 2011
Allosteric Supramolecular Coordination Constructs Lifschitz, Alejo M.; Rosen, Mari S.; McGuirk, C. Michael Journal of the American Chemical Society, Vol. 137, Issue 23 https://doi.org/10.1021/jacs.5b01054	journal	June 2015
Isolation and oxidation-reduction of methylviologen cation radicals. Novel disproportionation in charge-transfer salts by x-ray crystallography Bockman, T. M.; Kochi, J. K. The Journal of Organic Chemistry, Vol. 55, Issue 13, p. 4127-4135 https://doi.org/10.1021/jo00300a033	journal	June 1990
Uphill Photooxidation of NADH Analogues by Hexyl Viologen Catalyzed by Zinc Porphyrin-Linked Fullerenes ^† Fukuzumi, Shunichi; Imahori, Hiroshi; Okamoto, Ken The Journal of Physical Chemistry A, Vol. 106, Issue 10 https://doi.org/10.1021/jp011613g	journal	March 2002
Conformational Gating of Charge Separation in Porphyrin Oligomer-Fullerene Systems Gilbert, Mélina; Esdaile, Louisa J.; Hutin, Marie The Journal of Physical Chemistry C, Vol. 117, Issue 50 https://doi.org/10.1021/jp4098342	journal	December 2013
Ultrafast Conformational Dynamics of Electron Transfer in ExBox ⁴⁺ ⊂Perylene Young, Ryan M.; Dyar, Scott M.; Barnes, Jonathan C. The Journal of Physical Chemistry A, Vol. 117, Issue 47 https://doi.org/10.1021/jp409883a	journal	November 2013
Molecular basis of photoprotection and control of photosynthetic light-harvesting Pascal, Andrew A.; Liu, Zhenfeng; Broess, Koen Nature, Vol. 436, Issue 7047 https://doi.org/10.1038/nature03795	journal	July 2005
Lessons from nature about solar light harvesting Scholes, Gregory D.; Fleming, Graham R.; Olaya-Castro, Alexandra Nature Chemistry, Vol. 3, Issue 10 https://doi.org/10.1038/nchem.1145	journal	September 2011
Allosteric regulation and catalysis emerge via a common route Goodey, Nina M.; Benkovic, Stephen J. Nature Chemical Biology, Vol. 4, Issue 8 https://doi.org/10.1038/nchembio.98	journal	July 2008
An allosteric photoredox catalyst inspired by photosynthetic machinery Lifschitz, Alejo M.; Young, Ryan M.; Mendez-Arroyo, Jose Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7541	journal	March 2015
Self-regulation of photoinduced electron transfer by a molecular nonlinear transducer Straight, Stephen D.; Kodis, Gerdenis; Terazono, Yuichi Nature Nanotechnology, Vol. 3, Issue 5 https://doi.org/10.1038/nnano.2008.97	journal	May 2008
Electron and energy transfer modulation with photochromic switches Raymo, Fran�isco M.; Tomasulo, Massimiliano Chemical Society Reviews, Vol. 34, Issue 4 https://doi.org/10.1039/b400387j	journal	January 2005
Chemically regulating Rh( i )-Bodipy photoredox switches Lifschitz, A. M.; Young, R. M.; Mendez-Arroyo, J. Chem. Commun., Vol. 50, Issue 52 https://doi.org/10.1039/c4cc01345j	journal	January 2014
The PsbS Protein Controls the Organization of the Photosystem II Antenna in Higher Plant Thylakoid Membranes Kiss, Anett Z.; Ruban, Alexander V.; Horton, Peter Journal of Biological Chemistry, Vol. 283, Issue 7 https://doi.org/10.1074/jbc.M707410200	journal	November 2007
Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein Ahn, T. K.; Avenson, T. J.; Ballottari, M. Science, Vol. 320, Issue 5877 https://doi.org/10.1126/science.1154800	journal	May 2008

Cited By (6)

A Zn ₄ L ₆ Capsule with Enhanced Catalytic C−C Bond Formation Activity upon C ₆₀ Binding Lu, Zhenpin; Lavendomme, Roy; Burghaus, Olaf Angewandte Chemie, Vol. 131, Issue 27 https://doi.org/10.1002/ange.201903286	journal	May 2019
A Zn ₄ L ₆ Capsule with Enhanced Catalytic C−C Bond Formation Activity upon C ₆₀ Binding Lu, Zhenpin; Lavendomme, Roy; Burghaus, Olaf Angewandte Chemie International Edition, Vol. 58, Issue 27 https://doi.org/10.1002/anie.201903286	journal	May 2019
Coordination Booster‐Catalyst Assembly: Remote Osmium Outperforming Ruthenium in Boosting Catalytic Activity Mandal, Tanmoy; Singh, Vivek; Choudhury, Joyanta Chemistry – An Asian Journal, Vol. 14, Issue 24 https://doi.org/10.1002/asia.201901215	journal	October 2019
Modulation of the carboxamidine redox potential through photoinduced spiropyran or fulgimide isomerisation Andrews, M. Crawford; Peng, Ping; Rajput, Amit Photochemical & Photobiological Sciences, Vol. 17, Issue 4 https://doi.org/10.1039/c7pp00347a	journal	January 2018
A four-state fluorescent molecular switch Liu, Yuan; Zhou, Jiawang; Wasielewski, Michael R. Chemical Communications, Vol. 54, Issue 85 https://doi.org/10.1039/c8cc05159c	journal	January 2018
A Zn ₄ L ₆ Capsule with Enhanced Catalytic C−C Bond Formation Activity upon C ₆₀ Binding Lu, Zhenpin; Lavendomme, Roy; Burghaus, Olaf Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.39564	text	January 2019

Similar Records

An allosteric photoredox catalyst inspired by photosynthetic machinery

Journal Article · Sun Mar 29 20:00:00 EDT 2015 · Nature Communications · OSTI ID:1370514

Synthetic and Mechanistic Implications of Chlorine Photoelimination in Nickel/Photoredox C(sp³)–H Cross-Coupling

Journal Article · Thu Jan 28 19:00:00 EST 2021 · Accounts of Chemical Research · OSTI ID:1776559

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
bio-inspired
catalysis (heterogeneous)
catalysis (homogeneous)
charge transport
defects
electrodes - solar
hydrogen and fuel cells
materials and chemistry by design
membrane
optics
photosynthesis (natural and artificial)
solar (fuels)
solar (photovoltaic)
spin dynamics
synthesis (novel materials)
synthesis (self-assembly)

Cooperative Electronic and Structural Regulation in a Bioinspired Allosteric Photoredox Catalyst

Citation Formats

References (29)

Cited By (6)

Similar Records

Related Subjects