Mimicking Natural Photosynthesis: Designing Ultrafast Photosensitized Electron Transfer into Multiheme Cytochrome Protein Nanowires
Abstract
Efficient nanomaterials for artificial photosynthesis require fast and robust unidirectional electron transfer (ET) from photosensitizers through charge-separation and accumulation units to redox-active catalytic sites. We explored the ultrafast time-scale limits of photo-induced charge transfer between a Ru(II)tris(bipyridine) derivative photosensitizer and PpcA, a 3-heme c-type cytochrome serving as a nanoscale biological wire. Four covalent attachment sites (K28C, K29C, K52C, and G53C) were engineered in PpcA enabling site-specific covalent labeling with expected donor-acceptor (DA) distances of 4–8 Å. X-ray scattering results demonstrated that mutations and chemical labeling did not disrupt the structure of the proteins. Time-resolved spectroscopy revealed three orders of magnitude difference in charge transfer rates for the systems with otherwise similar DA distances and the same number of covalent bonds separating donors and acceptors. All-atom molecular dynamics simulations provided additional insight into the structure-function requirements for ultrafast charge transfer and the requirement of van der Waals contact between aromatic atoms of photosensitizers and hemes in order to observe sub-nanosecond ET. This work demonstrates opportunities to utilize multi-heme c-cytochromes as frameworks for designing ultrafast light-driven ET into charge-accumulating biohybrid model systems, and ultimately for mimicking the photosynthetic paradigm of efficiently coupling ultrafast, light-driven electron transfer chemistry to multi-step catalysis within small,more »
- Authors:
-
- James Madison Univ., Harrisonburg, VA (United States). Dept. of Chemistry and Biochemistry
- Argonne National Lab. (ANL), Argonne, IL (United States). Chemical Sciences and Engineering Div.
- James Madison Univ., Harrisonburg, VA (United States). Dept. of Biology
- Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Division
- Publication Date:
- Research Org.:
- Argonne National Laboratory (ANL), Argonne, IL (United States)
- Sponsoring Org.:
- National Science Foundation (NSF); USDOE Office of Science - Office of Basic Energy Sciences - Chemical Sciences, Geosciences, and Biosciences Division
- OSTI Identifier:
- 1779068
- Grant/Contract Number:
- AC02-06CH11357
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nanomaterials
- Additional Journal Information:
- Journal Volume: 10; Journal Issue: 11; Journal ID: ISSN 2079-4991
- Publisher:
- MDPI
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 36 MATERIALS SCIENCE; biohybrids; biomimetic photosynthesis; cytochrome c7; photo-induced electron transfer; ruthenium tris(bipyridine); ultrafast electron transfer
Citation Formats
Marzolf, Daniel R., McKenzie, Aidan M., O’Malley, Matthew C., Ponomarenko, Nina S., Swaim, Coleman M., Brittain, Tyler J., Simmons, Natalie L., Pokkuluri, Phani Raj, Mulfort, Karen L., Tiede, David M., and Kokhan, Oleksandr. Mimicking Natural Photosynthesis: Designing Ultrafast Photosensitized Electron Transfer into Multiheme Cytochrome Protein Nanowires. United States: N. p., 2020.
Web. doi:10.3390/nano10112143.
Marzolf, Daniel R., McKenzie, Aidan M., O’Malley, Matthew C., Ponomarenko, Nina S., Swaim, Coleman M., Brittain, Tyler J., Simmons, Natalie L., Pokkuluri, Phani Raj, Mulfort, Karen L., Tiede, David M., & Kokhan, Oleksandr. Mimicking Natural Photosynthesis: Designing Ultrafast Photosensitized Electron Transfer into Multiheme Cytochrome Protein Nanowires. United States. https://doi.org/10.3390/nano10112143
Marzolf, Daniel R., McKenzie, Aidan M., O’Malley, Matthew C., Ponomarenko, Nina S., Swaim, Coleman M., Brittain, Tyler J., Simmons, Natalie L., Pokkuluri, Phani Raj, Mulfort, Karen L., Tiede, David M., and Kokhan, Oleksandr. Wed .
"Mimicking Natural Photosynthesis: Designing Ultrafast Photosensitized Electron Transfer into Multiheme Cytochrome Protein Nanowires". United States. https://doi.org/10.3390/nano10112143. https://www.osti.gov/servlets/purl/1779068.
@article{osti_1779068,
title = {Mimicking Natural Photosynthesis: Designing Ultrafast Photosensitized Electron Transfer into Multiheme Cytochrome Protein Nanowires},
author = {Marzolf, Daniel R. and McKenzie, Aidan M. and O’Malley, Matthew C. and Ponomarenko, Nina S. and Swaim, Coleman M. and Brittain, Tyler J. and Simmons, Natalie L. and Pokkuluri, Phani Raj and Mulfort, Karen L. and Tiede, David M. and Kokhan, Oleksandr},
abstractNote = {Efficient nanomaterials for artificial photosynthesis require fast and robust unidirectional electron transfer (ET) from photosensitizers through charge-separation and accumulation units to redox-active catalytic sites. We explored the ultrafast time-scale limits of photo-induced charge transfer between a Ru(II)tris(bipyridine) derivative photosensitizer and PpcA, a 3-heme c-type cytochrome serving as a nanoscale biological wire. Four covalent attachment sites (K28C, K29C, K52C, and G53C) were engineered in PpcA enabling site-specific covalent labeling with expected donor-acceptor (DA) distances of 4–8 Å. X-ray scattering results demonstrated that mutations and chemical labeling did not disrupt the structure of the proteins. Time-resolved spectroscopy revealed three orders of magnitude difference in charge transfer rates for the systems with otherwise similar DA distances and the same number of covalent bonds separating donors and acceptors. All-atom molecular dynamics simulations provided additional insight into the structure-function requirements for ultrafast charge transfer and the requirement of van der Waals contact between aromatic atoms of photosensitizers and hemes in order to observe sub-nanosecond ET. This work demonstrates opportunities to utilize multi-heme c-cytochromes as frameworks for designing ultrafast light-driven ET into charge-accumulating biohybrid model systems, and ultimately for mimicking the photosynthetic paradigm of efficiently coupling ultrafast, light-driven electron transfer chemistry to multi-step catalysis within small, experimentally versatile photosynthetic biohybrid assemblies.},
doi = {10.3390/nano10112143},
journal = {Nanomaterials},
number = 11,
volume = 10,
place = {United States},
year = {Wed Oct 28 00:00:00 EDT 2020},
month = {Wed Oct 28 00:00:00 EDT 2020}
}
Works referenced in this record:
Fragment charge difference method for estimating donor–acceptor electronic coupling: Application to DNA π-stacks
journal, September 2002
- Voityuk, Alexander A.; Rösch, Notker
- The Journal of Chemical Physics, Vol. 117, Issue 12
Electron transfer in ruthenium-modified proteins
journal, May 1992
- Winkler, Jay R.; Gray, Harry B.
- Chemical Reviews, Vol. 92, Issue 3
Approximately diabatic states from block diagonalization of the electronic Hamiltonian
journal, December 1988
- Pacher, T.; Cederbaum, L. S.; Köppel, H.
- The Journal of Chemical Physics, Vol. 89, Issue 12
Energy Flow in Proteins
journal, May 2008
- Leitner, David M.
- Annual Review of Physical Chemistry, Vol. 59, Issue 1
Vibrational Energy Relaxation of “Tailored” Hemes in Myoglobin Following Ligand Photolysis Supports Energy Funneling Mechanism of Heme “Cooling”
journal, September 2003
- Bu, Lintao; Straub, John E.
- The Journal of Physical Chemistry B, Vol. 107, Issue 38
Supramolecular Cobaloxime Assemblies for H 2 Photocatalysis: An Initial Solution State Structure−Function Analysis †
journal, November 2010
- Mulfort, Karen L.; Tiede, David M.
- The Journal of Physical Chemistry B, Vol. 114, Issue 45
Ultrafast Heme Dynamics in Ferrous versus Ferric Cytochrome c Studied by Time-Resolved Resonance Raman and Transient Absorption Spectroscopy
journal, June 2006
- Negrerie, Michel; Cianetti, Simona; Vos, Marten H.
- The Journal of Physical Chemistry B, Vol. 110, Issue 25
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
Nature of biological electron transfer
journal, February 1992
- Moser, Christopher C.; Keske, Jonathan M.; Warncke, Kurt
- Nature, Vol. 355, Issue 6363
Evidence for interaction between the triheme cytochrome PpcA from Geobacter sulfurreducens and anthrahydroquinone-2,6-disulfonate, an analog of the redox active components of humic substances
journal, June 2014
- Dantas, Joana M.; Morgado, Leonor; Catarino, Teresa
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1837, Issue 6
Photoinduced electron transfer between cytochrome c peroxidase and yeast cytochrome c labeled at Cys 102 with (4-bromomethyl-4'-methylbipyridine)[bis(bipyridine)]ruthenium2+
journal, October 1991
- Geren, Lois; Hahm, Seung; Durham, Bill
- Biochemistry, Vol. 30, Issue 39
Direct Observation of Protein Vibrations by Selective Incorporation of Spectroscopically Observable Carbon−Deuterium Bonds in Cytochrome c
journal, March 2001
- Chin, Jodie K.; Jimenez, Ralph; Romesberg, Floyd E.
- Journal of the American Chemical Society, Vol. 123, Issue 10
Overproduction of theBradyrhizobium japonicum c-Type Cytochrome Subunits of thecbb3Oxidase inEscherichia coli
journal, October 1998
- Arslan, Engin; Schulz, Henk; Zufferey, Rachel
- Biochemical and Biophysical Research Communications, Vol. 251, Issue 3
Scalable molecular dynamics with NAMD
journal, January 2005
- Phillips, James C.; Braun, Rosemary; Wang, Wei
- Journal of Computational Chemistry, Vol. 26, Issue 16, p. 1781-1802
Nanosecond Photoreduction of Cytochrome P450cam by Channel-Specific Ru-diimine Electron Tunneling Wires
journal, October 2003
- Dunn, Alexander R.; Dmochowski, Ivan J.; Winkler, Jay R.
- Journal of the American Chemical Society, Vol. 125, Issue 41
Semisynthesis of bipyridyl-alanine cytochrome c mutants: novel proteins with enhanced electron-transfer properties
journal, September 1993
- Wuttke, Deborah S.; Gray, Harry B.; Fisher, Stewart L.
- Journal of the American Chemical Society, Vol. 115, Issue 18
Structural insights into the modulation of the redox properties of two Geobacter sulfurreducens homologous triheme cytochromes
journal, September 2008
- Morgado, Leonor; Bruix, Marta; Orshonsky, Valerie
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1777, Issue 9
Ballistic and diffusive vibrational energy transport in molecules
journal, January 2019
- Rubtsov, Igor V.; Burin, Alexander L.
- The Journal of Chemical Physics, Vol. 150, Issue 2
Vibrational energy flow across heme–cytochrome c and cytochrome c–water interfaces
journal, May 2014
- Agbo, Johnson K.; Xu, Yao; Zhang, Ping
- Theoretical Chemistry Accounts, Vol. 133, Issue 7
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
- Ponomarenko, Nina S.; Kokhan, Oleksandr; Pokkuluri, Phani R.
- Photosynthesis Research, Vol. 143, Issue 2
Long-Range Electron Tunneling
journal, February 2014
- Winkler, Jay R.; Gray, Harry B.
- Journal of the American Chemical Society, Vol. 136, Issue 8
Vibrational Energy Transfer from Heme through Atomic Contacts in Proteins
journal, May 2018
- Yamashita, Satoshi; Mizuno, Misao; Tran, Duy Phuoc
- The Journal of Physical Chemistry B, Vol. 122, Issue 22
Natural engineering principles of electron tunnelling in biological oxidation–reduction
journal, November 1999
- Page, Christopher C.; Moser, Christopher C.; Chen, Xiaoxi
- Nature, Vol. 402, Issue 6757
Calculation of electronic coupling matrix elements for ground and excited state electron transfer reactions: Comparison of the generalized Mulliken–Hush and block diagonalization methods
journal, June 1997
- Cave, Robert J.; Newton, Marshall D.
- The Journal of Chemical Physics, Vol. 106, Issue 22
Redox Characterization of Geobacter sulfurreducens Cytochrome c 7 : Physiological Relevance of the Conserved Residue F15 Probed by Site-Specific Mutagenesis †
journal, August 2004
- Pessanha, Miguel; Londer, Yuri Y.; Long, W. Chris
- Biochemistry, Vol. 43, Issue 30
Photoinduced Oxidation of Horseradish Peroxidase
journal, March 1997
- Berglund, Johan; Pascher, Torbjörn; Winkler, Jay R.
- Journal of the American Chemical Society, Vol. 119, Issue 10
Electron-Tunneling Pathways in Oroteins
journal, December 1992
- Beratan, David N.; Onuchic, José Nelson; Winkler, Jay R.
- Science, Vol. 258, Issue 5089, p. 1740-1741
The Nature of Aqueous Tunneling Pathways Between Electron-Transfer Proteins
journal, November 2005
- Lin, J.
- Science, Vol. 310, Issue 5752
Picosecond Optical Thermometry of Protein in H 2 O
journal, March 2007
- Marcus, George A.; Schwettman, H. Alan
- The Journal of Physical Chemistry B, Vol. 111, Issue 11
Bidirectional Photoinduced Electron Transfer in Ruthenium(II)-Tris-bipyridyl-Modified PpcA, a Multi-heme c -Type Cytochrome from Geobacter sulfurreducens
journal, December 2014
- Kokhan, Oleksandr; Ponomarenko, Nina S.; Pokkuluri, P. Raj
- The Journal of Physical Chemistry B, Vol. 119, Issue 24
Electron tunneling through sensitizer wires bound to proteins
journal, February 2010
- Hartings, Matthew R.; Kurnikov, Igor V.; Dunn, Alexander R.
- Coordination Chemistry Reviews, Vol. 254, Issue 3-4
Femtosecond UV Studies of the Electronic Relaxation Processes in Cytochrome c
journal, November 2011
- Bräm, Olivier; Consani, Cristina; Cannizzo, Andrea
- The Journal of Physical Chemistry B, Vol. 115, Issue 46
Importance of Atomic Contacts in Vibrational Energy Flow in Proteins
journal, May 2016
- Kondoh, Masato; Mizuno, Misao; Mizutani, Yasuhisa
- The Journal of Physical Chemistry Letters, Vol. 7, Issue 11
Photoinduced electron-transfer kinetics of singly labeled ruthenium bis(bipyridine) dicarboxybipyridine cytochrome c derivatives
journal, October 1989
- Durham, Bill; Pan, Lian Ping; Long, Joan E.
- Biochemistry, Vol. 28, Issue 21
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
Multimerization of Solution-State Proteins by Tetrakis(4-sulfonatophenyl)porphyrin
journal, July 2014
- Kokhan, Oleksandr; Ponomarenko, Nina; Pokkuluri, P. Raj
- Biochemistry, Vol. 53, Issue 31
Preparation and characterization of singly labeled ruthenium polypyridine cytochrome c derivatives
journal, September 1988
- Pan, Lian Ping; Durham, Bill; Wolinska, Justyna
- Biochemistry, Vol. 27, Issue 19
Redox- and pH-linked conformational changes in triheme cytochrome PpcA from Geobacter sulfurreducens
journal, January 2017
- Morgado, Leonor; Bruix, Marta; Pokkuluri, P. Raj
- Biochemical Journal, Vol. 474, Issue 2
High-driving-force electron transfer in metalloproteins: intramolecular oxidation of ferrocytochrome c by Ru(2,2'-bpy)2(im)(his-33)3+
journal, August 1991
- Chang, I. Jy; Gray, Harry B.; Winkler, Jay R.
- Journal of the American Chemical Society, Vol. 113, Issue 18
Vibrational Energy Transfer and Heat Conduction in a Protein
journal, February 2003
- Yu, Xin; Leitner, David M.
- The Journal of Physical Chemistry B, Vol. 107, Issue 7
Comparing Photosynthetic and Photovoltaic Efficiencies and Recognizing the Potential for Improvement
journal, May 2011
- Blankenship, R. E.; Tiede, D. M.; Barber, J.
- Science, Vol. 332, Issue 6031, p. 805-809
Thermodynamic Characterization of a Triheme Cytochrome Family from Geobacter sulfurreducens Reveals Mechanistic and Functional Diversity
journal, July 2010
- Morgado, Leonor; Bruix, Marta; Pessanha, Miguel
- Biophysical Journal, Vol. 99, Issue 1
Oxygenic photosynthesis: history, status and perspective
journal, January 2019
- Junge, Wolfgang
- Quarterly Reviews of Biophysics, Vol. 52
Ultrafast Light-Driven Electron Transfer in a Ru(II)tris(bipyridine)-Labeled Multiheme Cytochrome
journal, August 2019
- van Wonderen, Jessica H.; Hall, Christopher R.; Jiang, Xiuyun
- Journal of the American Chemical Society, Vol. 141, Issue 38
Production of Liquid Solar Fuels and Their Use in Fuel Cells
journal, December 2017
- Fukuzumi, Shunichi
- Joule, Vol. 1, Issue 4
Vibrational energy relaxation in proteins
journal, March 2005
- Fujisaki, H.; Straub, J. E.
- Proceedings of the National Academy of Sciences, Vol. 102, Issue 19
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
Electron-Tunneling Pathways in Cytochrome c
journal, May 1992
- Wuttke, D. S.; Bjerrum, M. J.; Winkler, J. R.
- Science, Vol. 256, Issue 5059
Structure of a novel c 7 -type three-heme cytochrome domain from a multidomain cytochrome c polymer
journal, June 2004
- Pokkuluri, P. Raj; Londer, Yuri Y.; Duke, Norma E. C.
- Protein Science, Vol. 13, Issue 6
Observing Vibrational Energy Flow in a Protein with the Spatial Resolution of a Single Amino Acid Residue
journal, September 2014
- Fujii, Naoki; Mizuno, Misao; Ishikawa, Haruto
- The Journal of Physical Chemistry Letters, Vol. 5, Issue 18
Artificial Photosynthesis for Solar Fuels – an Evolving Research Field within AMPEA, a Joint Programme of the European Energy Research Alliance
journal, January 2013
- Thapper, Anders; Styring, Stenbjörn; Saracco, Guido
- Green, Vol. 3, Issue 1
New Hamiltonian model for long-range electronic superexchange in complex molecular structures
journal, May 1993
- Gruschus, James M.; Kuki, Atsuo
- The Journal of Physical Chemistry, Vol. 97, Issue 21
Intramolecular Vibrational Preparation of the Unfolding Transition State of Zn II -Substituted Cytochrome c
journal, November 2006
- Lampa-Pastirk, Sanela; Beck, Warren F.
- The Journal of Physical Chemistry B, Vol. 110, Issue 46
Direct observations of ligand dynamics in hemoglobin by subpicosecond infrared spectroscopy.
journal, November 1989
- Anfinrud, P. A.; Han, C.; Hochstrasser, R. M.
- Proceedings of the National Academy of Sciences, Vol. 86, Issue 21
Electron Flow through Nitrotyrosinate in Pseudomonas aeruginosa Azurin
journal, July 2013
- Warren, Jeffrey J.; Herrera, Nadia; Hill, Michael G.
- Journal of the American Chemical Society, Vol. 135, Issue 30
Electron Flow through Metalloproteins
journal, November 2013
- Winkler, Jay R.; Gray, Harry B.
- Chemical Reviews, Vol. 114, Issue 7
Femtosecond processes in proteins
journal, April 1999
- Vos, Marten H.; Martin, Jean-Louis
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1411, Issue 1
Molecular Dynamics Study on the Solvent Dependent Heme Cooling Following Ligand Photolysis in Carbonmonoxy Myoglobin
journal, March 2007
- Zhang, Yong; Fujisaki, Hiroshi; Straub, John E.
- The Journal of Physical Chemistry B, Vol. 111, Issue 12
Protein electron transfer rates set by the bridging secondary and tertiary structure
journal, May 1991
- Beratan, D.; Betts, J.; Onuchic, J.
- Science, Vol. 252, Issue 5010
The O 2 -Evolving Complex of Photosystem II: Recent Insights from Quantum Mechanics/Molecular Mechanics (QM/MM), Extended X-ray Absorption Fine Structure (EXAFS), and Femtosecond X-ray Crystallography Data
journal, December 2016
- Askerka, Mikhail; Brudvig, Gary W.; Batista, Victor S.
- Accounts of Chemical Research, Vol. 50, Issue 1
Redox-linked conformational changes of a multiheme cytochrome from Geobacter sulfurreducens
journal, August 2007
- Morgado, Leonor; Bruix, Marta; Londer, Yuri Y.
- Biochemical and Biophysical Research Communications, Vol. 360, Issue 1
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
Ellipsoidal Delocalization of Tunneling Electrons in Long-Range Electron Transfer Proteins
journal, December 1999
- Gruschus, James M.; Kuki, Atsuo
- The Journal of Physical Chemistry B, Vol. 103, Issue 51
Artificial photosynthesis as a frontier technology for energy sustainability
journal, January 2013
- Faunce, Thomas; Styring, Stenbjorn; Wasielewski, Michael R.
- Energy & Environmental Science, Vol. 6, Issue 4
Direct Observation of Vibrational Energy Flow in Cytochrome c
journal, November 2011
- Fujii, Naoki; Mizuno, Misao; Mizutani, Yasuhisa
- The Journal of Physical Chemistry B, Vol. 115, Issue 44
Vibrational Energy Transport in Molecules Studied by Relaxation-Assisted Two-Dimensional Infrared Spectroscopy
journal, April 2015
- Rubtsova, Natalia I.; Rubtsov, Igor V.
- Annual Review of Physical Chemistry, Vol. 66, Issue 1
Direct observation of global protein motion in hemoglobin and myoglobin on picosecond time scales
journal, March 1991
- Genberg, L.; Richard, L.; McLendon, G.
- Science, Vol. 251, Issue 4997
Rates of Heme Oxidation and Reduction in Ru(His33)cytochrome c at Very High Driving Forces
journal, January 1996
- Mines, Gary A.; Bjerrum, Morten J.; Hill, Michael G.
- Journal of the American Chemical Society, Vol. 118, Issue 8
Detection of a charge-separated catalyst precursor state in a linked photosensitizer-catalyst assembly
journal, January 2013
- Mukherjee, Anusree; Kokhan, Oleksandr; Huang, Jier
- Physical Chemistry Chemical Physics, Vol. 15, Issue 48
Charge Transfer in Dynamical Biosystems, or The Treachery of (Static) Images
journal, October 2014
- Beratan, David N.; Liu, Chaoren; Migliore, Agostino
- Accounts of Chemical Research, Vol. 48, Issue 2
Electron tunneling in respiratory complex I
journal, October 2010
- Hayashi, T.; Stuchebrukhov, A. A.
- Proceedings of the National Academy of Sciences, Vol. 107, Issue 45
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
Electronic coupling matrix elements from charge constrained density functional theory calculations using a plane wave basis set
journal, December 2010
- Oberhofer, Harald; Blumberger, Jochen
- The Journal of Chemical Physics, Vol. 133, Issue 24
Interprotein electron transfer biohybrid system for photocatalytic H2 production
journal, January 2020
- Brahmachari, Udita; Pokkuluri, P. Raj; Tiede, David M.
- Photosynthesis Research, Vol. 143, Issue 2
Water oxidation in photosystem II
journal, June 2019
- Lubitz, Wolfgang; Chrysina, Maria; Cox, Nicholas
- Photosynthesis Research, Vol. 142, Issue 1
Intramolecular Vibrational Excitation of Unfolding Reactions in Zn II -Substituted and Metal-Free Cytochromes c : Activation Enthalpies from Integrated Fluorescence Stokes Shift and Line Shape Excitation Profiles
journal, October 2008
- Barns, Kenneth J.; Lampa-Pastirk, Sanela; Dillman, Kevin L.
- The Journal of Physical Chemistry B, Vol. 112, Issue 47
Photosynthetic energy conversion: natural and artificial
journal, January 2009
- Barber, James
- Chem. Soc. Rev., Vol. 38, Issue 1
Thermodynamic Characterization of Triheme Cytochrome PpcA from Geobacter sulfurreducens : Evidence for a Role Played in e - /H + Energy Transduction † , ‡
journal, November 2006
- Pessanha, Miguel; Morgado, Leonor; Louro, Ricardo O.
- Biochemistry, Vol. 45, Issue 46
Design of a Ruthenium-Labeled Cytochrome c Derivative to Study Electron Transfer with the Cytochrome bc 1 Complex †
journal, March 2003
- Engstrom, Gregory; Rajagukguk, Ray; Saunders, Aleister J.
- Biochemistry, Vol. 42, Issue 10
Energy Flow from Solute to Solvent Probed by Femtosecond IR Spectroscopy: Malachite Green and Heme Protein Solutions
journal, November 1994
- Lian, Tianquan; Locke, Bruce; Kholodenko, Yuriy
- The Journal of Physical Chemistry, Vol. 98, Issue 45
VMD: Visual molecular dynamics
journal, February 1996
- Humphrey, William; Dalke, Andrew; Schulten, Klaus
- Journal of Molecular Graphics, Vol. 14, Issue 1
UV Resonance Raman Investigations of Peptide and Protein Structure and Dynamics
journal, February 2012
- Oladepo, Sulayman A.; Xiong, Kan; Hong, Zhenmin
- Chemical Reviews, Vol. 112, Issue 5
Evaluation of Electronic Coupling in Transition-Metal Systems Using DFT: Application to the Hexa-Aquo Ferric−Ferrous Redox Couple
journal, January 2009
- Migliore, Agostino; Sit, Patrick H. -L.; Klein, Michael L.
- Journal of Chemical Theory and Computation, Vol. 5, Issue 2
Configuration interaction based on constrained density functional theory: A multireference method
journal, October 2007
- Wu, Qin; Cheng, Chiao-Lun; Van Voorhis, Troy
- The Journal of Chemical Physics, Vol. 127, Issue 16
Picosecond Photoreduction of Inducible Nitric Oxide Synthase by Rhenium(I)−Diimine Wires
journal, November 2005
- Belliston-Bittner, Wendy; Dunn, Alexander R.; Nguyen, Yen Hoang Le
- Journal of the American Chemical Society, Vol. 127, Issue 45