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Title: 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 » experimentally versatile photosynthetic biohybrid assemblies.« less

Authors:
 [1];  [1];  [1];  [2];  [1];  [1];  [3];  [4];  [2];  [2]; ORCiD logo [1]
  1. James Madison Univ., Harrisonburg, VA (United States). Dept. of Chemistry and Biochemistry
  2. Argonne National Lab. (ANL), Argonne, IL (United States). Chemical Sciences and Engineering Div.
  3. James Madison Univ., Harrisonburg, VA (United States). Dept. of Biology
  4. 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}
}

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