skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Microenvironment control of porphyrin binding, organization, and function in peptide nanofiber assemblies

Abstract

To take peptide materials from predominantly structural to functional assemblies, variations in cofactor binding sites must be engineered and controlled. Here, we have employed the peptide sequence c16-AHX3K3-CO2H where X3 represents the aliphatic structural component of the peptide design that dictates β-sheet formation and upon self-assembly yields a change in the overall microenvironment surrounding the Zn protoporphyrin IX ((PPIX)Zn) binding site. All peptides studied yield β-sheet rich nanofibers highlighting the materials’ resiliency to amino acid substitution. We highlight that the (PPIX)Zn binding constants correlate strongly with amino acid side chain volume, where X = L or I yields the lowest dissociation constant values (KD). The resulting microenvironment highlights the materials’ ability to control interchromophore electronic interactions such that slip-stacked cofacial arrangements are observed via exciton splitting in UV/visible and circular dichroism spectroscopy. Steady state and time-resolved photoluminescence suggests that greater interchromophore packing yields larger excimer populations and corresponding longer excimer association lifetimes (τA) which directly translates to shorter exciton diffusion lengths. In comparison to synthetic porphyrin molecular assemblies, this work demonstrates the ability to employ the peptide assembly to modulate the degree of cofactor arrangement, extent of excimer formation, and the exciton hopping rates all while in a platform amenablemore » for producing polymer-like material« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [1]; ORCiD logo [1];  [1]; ORCiD logo [2]; ORCiD logo [1]
  1. Argonne National Lab. (ANL), Lemont, IL (United States). Center for Nanoscale Materials
  2. Argonne National Lab. (ANL), Lemont, IL (United States). Center for Nanoscale Materials; Northwestern Univ., Evanston, IL (United States). Dept. of Chemistry
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division
OSTI Identifier:
1542129
Alternate Identifier(s):
OSTI ID: 1498806
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Nanoscale
Additional Journal Information:
Journal Volume: 11; Journal Issue: 12; Journal ID: ISSN 2040-3364
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
63 RADIATION, THERMAL, AND OTHER ENVIRON. POLLUTANT EFFECTS ON LIVING ORGS. AND BIOL. MAT.; 14 SOLAR ENERGY

Citation Formats

Solomon, Lee A., Wood, Anna R., Sykes, Matthew E., Diroll, Benjamin T., Wiederrecht, Gary P., Schaller, Richard D., and Fry, H. Christopher. Microenvironment control of porphyrin binding, organization, and function in peptide nanofiber assemblies. United States: N. p., 2019. Web. https://doi.org/10.1039/c8nr09556f.
Solomon, Lee A., Wood, Anna R., Sykes, Matthew E., Diroll, Benjamin T., Wiederrecht, Gary P., Schaller, Richard D., & Fry, H. Christopher. Microenvironment control of porphyrin binding, organization, and function in peptide nanofiber assemblies. United States. https://doi.org/10.1039/c8nr09556f
Solomon, Lee A., Wood, Anna R., Sykes, Matthew E., Diroll, Benjamin T., Wiederrecht, Gary P., Schaller, Richard D., and Fry, H. Christopher. Thu . "Microenvironment control of porphyrin binding, organization, and function in peptide nanofiber assemblies". United States. https://doi.org/10.1039/c8nr09556f. https://www.osti.gov/servlets/purl/1542129.
@article{osti_1542129,
title = {Microenvironment control of porphyrin binding, organization, and function in peptide nanofiber assemblies},
author = {Solomon, Lee A. and Wood, Anna R. and Sykes, Matthew E. and Diroll, Benjamin T. and Wiederrecht, Gary P. and Schaller, Richard D. and Fry, H. Christopher},
abstractNote = {To take peptide materials from predominantly structural to functional assemblies, variations in cofactor binding sites must be engineered and controlled. Here, we have employed the peptide sequence c16-AHX3K3-CO2H where X3 represents the aliphatic structural component of the peptide design that dictates β-sheet formation and upon self-assembly yields a change in the overall microenvironment surrounding the Zn protoporphyrin IX ((PPIX)Zn) binding site. All peptides studied yield β-sheet rich nanofibers highlighting the materials’ resiliency to amino acid substitution. We highlight that the (PPIX)Zn binding constants correlate strongly with amino acid side chain volume, where X = L or I yields the lowest dissociation constant values (KD). The resulting microenvironment highlights the materials’ ability to control interchromophore electronic interactions such that slip-stacked cofacial arrangements are observed via exciton splitting in UV/visible and circular dichroism spectroscopy. Steady state and time-resolved photoluminescence suggests that greater interchromophore packing yields larger excimer populations and corresponding longer excimer association lifetimes (τA) which directly translates to shorter exciton diffusion lengths. In comparison to synthetic porphyrin molecular assemblies, this work demonstrates the ability to employ the peptide assembly to modulate the degree of cofactor arrangement, extent of excimer formation, and the exciton hopping rates all while in a platform amenable for producing polymer-like material},
doi = {10.1039/c8nr09556f},
journal = {Nanoscale},
number = 12,
volume = 11,
place = {United States},
year = {2019},
month = {3}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Molecular–Supramolecular Light Harvesting for Photochemical Energy Conversion: Making Every Photon Count
journal, January 2017


The crystal structure of the light-harvesting complex II (B800–850) from Rhodospirillum molischianum
journal, May 1996


Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å
journal, April 2011

  • Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren
  • Nature, Vol. 473, Issue 7345
  • DOI: 10.1038/nature09913

Supramolecular organization of thylakoid membrane proteins in green plants
journal, January 2005

  • Dekker, Jan P.; Boekema, Egbert J.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 1-2
  • DOI: 10.1016/j.bbabio.2004.09.009

Supramolecular organization of photosystem II in green plants
journal, January 2012

  • Kouřil, Roman; Dekker, Jan P.; Boekema, Egbert J.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1817, Issue 1
  • DOI: 10.1016/j.bbabio.2011.05.024

Photocurrent activity of light-harvesting complex II isolated from spinach and its pigments in dye-sensitized TiO2 solar cell
journal, December 2013


Improved Device Performance of Polymer Solar Cells by Using a Thin Light-harvesting-Complex Modified ZnO Film as the Cathode Interlayer
journal, August 2015

  • Liu, Xiaohui; Liu, Cheng; Sun, Ruixue
  • ACS Applied Materials & Interfaces, Vol. 7, Issue 34
  • DOI: 10.1021/acsami.5b05969

Self-assembled porphyrin nanostructures
journal, January 2009

  • Medforth, Craig John; Wang, Zhongchun; Martin, Kathleen Ewing
  • Chemical Communications, Issue 47
  • DOI: 10.1039/b914432c

Self-Assembly Strategies for Integrating Light Harvesting and Charge Separation in Artificial Photosynthetic Systems
journal, December 2009

  • Wasielewski, Michael R.
  • Accounts of Chemical Research, Vol. 42, Issue 12
  • DOI: 10.1021/ar9001735

Supramolecular approach towards light-harvesting materials based on porphyrins and chlorophylls
journal, January 2018


Hemoprotein-based supramolecular assembling systems
journal, April 2014


Peptide-Modulated Self-Assembly of Chromophores toward Biomimetic Light-Harvesting Nanoarchitectonics
journal, August 2015


Self-Assembly of Highly Ordered Peptide Amphiphile Metalloporphyrin Arrays
journal, August 2012

  • Fry, H. Christopher; Garcia, Jamie M.; Medina, Matthew J.
  • Journal of the American Chemical Society, Vol. 134, Issue 36
  • DOI: 10.1021/ja304674d

Tailorable Exciton Transport in Doped Peptide–Amphiphile Assemblies
journal, August 2017


Volumes of Individual Amino Acid Residues in Gas-Phase Peptide Ions
journal, April 1999

  • Counterman, Anne E.; Clemmer, David E.
  • Journal of the American Chemical Society, Vol. 121, Issue 16
  • DOI: 10.1021/ja984344p

Zinc-binding structure of a catalytic amyloid from solid-state NMR
journal, May 2017

  • Lee, Myungwoon; Wang, Tuo; Makhlynets, Olga V.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 24
  • DOI: 10.1073/pnas.1706179114

Geometric constraints for porphyrin binding in helical protein binding sites
journal, February 2009

  • Negron, Christopher; Fufezan, Christian; Koder, Ronald L.
  • Proteins: Structure, Function, and Bioinformatics, Vol. 74, Issue 2
  • DOI: 10.1002/prot.22143

Fourier Transform Infrared Spectroscopic Analysis of Protein Secondary Structures
journal, August 2007


How to study proteins by circular dichroism
journal, August 2005

  • Kelly, Sharon M.; Jess, Thomas J.; Price, Nicholas C.
  • Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics, Vol. 1751, Issue 2
  • DOI: 10.1016/j.bbapap.2005.06.005

Heme Protein Assemblies
journal, February 2004

  • Reedy, Charles J.; Gibney, Brian R.
  • Chemical Reviews, Vol. 104, Issue 2
  • DOI: 10.1021/cr0206115

Computational de Novo Design and Characterization of a Protein That Selectively Binds a Highly Hyperpolarizable Abiological Chromophore
journal, September 2013

  • Fry, H. Christopher; Lehmann, Andreas; Sinks, Louise E.
  • Journal of the American Chemical Society, Vol. 135, Issue 37
  • DOI: 10.1021/ja4067404

Photoinduced Electron Transfer Elicits a Change in the Static Dielectric Constant of a de Novo Designed Protein
journal, February 2016

  • Polizzi, Nicholas F.; Eibling, Matthew J.; Perez-Aguilar, Jose Manuel
  • Journal of the American Chemical Society, Vol. 138, Issue 7
  • DOI: 10.1021/jacs.5b13180

De novo design of a hyperstable non-natural protein–ligand complex with sub-Å accuracy
journal, August 2017

  • Polizzi, Nicholas F.; Wu, Yibing; Lemmin, Thomas
  • Nature Chemistry, Vol. 9, Issue 12
  • DOI: 10.1038/nchem.2846

Effect of Four Helix Bundle Topology on Heme Binding and Redox Properties
journal, March 1998

  • Gibney, Brian R.; Rabanal, Francesc; Reddy, Konda S.
  • Biochemistry, Vol. 37, Issue 13
  • DOI: 10.1021/bi971856s

Design of Amphiphilic Protein Maquettes:  Controlling Assembly, Membrane Insertion, and Cofactor Interactions
journal, September 2005

  • Discher, Bohdana M.; Noy, Dror; Strzalka, Joseph
  • Biochemistry, Vol. 44, Issue 37
  • DOI: 10.1021/bi050695m

Computational De Novo Design and Characterization of a Four-Helix Bundle Protein that Selectively Binds a Nonbiological Cofactor
journal, February 2005

  • Cochran, Frank V.; Wu, Sophia P.; Wang, Wei
  • Journal of the American Chemical Society, Vol. 127, Issue 5
  • DOI: 10.1021/ja044129a

De Novo Design of a Single-Chain Diphenylporphyrin Metalloprotein
journal, September 2007

  • Bender, Gretchen M.; Lehmann, Andreas; Zou, Hongling
  • Journal of the American Chemical Society, Vol. 129, Issue 35
  • DOI: 10.1021/ja071199j

Using α-Helical Coiled-Coils to Design Nanostructured Metalloporphyrin Arrays
journal, September 2008

  • McAllister, Karen A.; Zou, Hongling; Cochran, Frank V.
  • Journal of the American Chemical Society, Vol. 130, Issue 36
  • DOI: 10.1021/ja800697g

Computational Design and Elaboration of a de Novo Heterotetrameric α-Helical Protein That Selectively Binds an Emissive Abiological (Porphinato)zinc Chromophore
journal, March 2010

  • Fry, H. Christopher; Lehmann, Andreas; Saven, Jeffery G.
  • Journal of the American Chemical Society, Vol. 132, Issue 11
  • DOI: 10.1021/ja907407m

Design and engineering of water-soluble light-harvesting protein maquettes
journal, January 2017

  • Kodali, Goutham; Mancini, Joshua A.; Solomon, Lee A.
  • Chemical Science, Vol. 8, Issue 1
  • DOI: 10.1039/C6SC02417C

Transcriptomic and Physiological Evidence for the Relationship between Unsaturated Fatty Acid and Salt Stress in Peanut
journal, January 2018


The role of intramolecular interactions in the functional control of multiheme cytochromes c
journal, August 2011


Peptide Arrays: Development and Application
journal, December 2017


Integration of Layered Redox Proteins and Conductive Supports for Bioelectronic Applications
journal, April 2000


Self-assembly of peptide amphiphiles: From molecules to nanostructures to biomaterials
journal, January 2010

  • Cui, Honggang; Webber, Matthew J.; Stupp, Samuel I.
  • Biopolymers, Vol. 94, Issue 1, p. 1-18
  • DOI: 10.1002/bip.21328

Artificial photosynthetic systems: assemblies of slipped cofacial porphyrins and phthalocyanines showing strong electronic coupling
journal, January 2007

  • Satake, Akiharu; Kobuke, Yoshiaki
  • Organic & Biomolecular Chemistry, Vol. 5, Issue 11
  • DOI: 10.1039/b703405a

Structural Studies by Exciton Coupled Circular Dichroism over a Large Distance:  Porphyrin Derivatives of Steroids, Dimeric Steroids, and Brevetoxin B
journal, January 1996

  • Matile, Stefan; Berova, Nina; Nakanishi, Koji
  • Journal of the American Chemical Society, Vol. 118, Issue 22
  • DOI: 10.1021/ja960126p

Application of electronic circular dichroism in configurational and conformational analysis of organic compounds
journal, January 2007

  • Berova, Nina; Bari, Lorenzo Di; Pescitelli, Gennaro
  • Chemical Society Reviews, Vol. 36, Issue 6
  • DOI: 10.1039/b515476f

Structure-Based Calculations of the Optical Spectra of the LH2 Bacteriochlorophyll-Protein Complex from Rhodopseudomonas acidophila
journal, September 1996


Structure-Based Calculations of Optical Spectra of Photosystem I Suggest an Asymmetric Light-Harvesting Process
journal, March 2010

  • Adolphs, Julian; Müh, Frank; Madjet, Mohamed El-Amine
  • Journal of the American Chemical Society, Vol. 132, Issue 10
  • DOI: 10.1021/ja9072222

Tailoring Porphyrins and Chlorins for Self-Assembly in Biomimetic Artificial Antenna Systems
journal, August 2005

  • Balaban, Teodor Silviu
  • Accounts of Chemical Research, Vol. 38, Issue 8
  • DOI: 10.1021/ar040211z

Porphyrin-sensitized solar cells
journal, January 2013

  • Li, Lu-Lin; Diau, Eric Wei-Guang
  • Chem. Soc. Rev., Vol. 42, Issue 1
  • DOI: 10.1039/C2CS35257E

Glycosylated Porphyrins, Phthalocyanines, and Other Porphyrinoids for Diagnostics and Therapeutics
journal, August 2015

  • Singh, Sunaina; Aggarwal, Amit; Bhupathiraju, N. V. S. Dinesh K.
  • Chemical Reviews, Vol. 115, Issue 18
  • DOI: 10.1021/acs.chemrev.5b00244

Ultrafast Relaxation of Zinc Protoporphyrin Encapsulated within Apomyoglobin in Buffer Solutions
journal, July 2007

  • Luo, Liyang; Chang, Chin-Hao; Chen, Yue-Ching
  • The Journal of Physical Chemistry B, Vol. 111, Issue 26
  • DOI: 10.1021/jp068449n

Discrete Cyclic Porphyrin Arrays as Artificial Light-Harvesting Antenna
journal, December 2009

  • Aratani, Naoki; Kim, Dongho; Osuka, Atsuhiro
  • Accounts of Chemical Research, Vol. 42, Issue 12
  • DOI: 10.1021/ar9001697

Heme Protein Assemblies
journal, May 2004


Inulinase Immobilized Lectin Affinity Magnetic Nanoparticles for Inulin Hydrolysis
journal, January 2021

  • Kilimci, Ulviye; Evli, Sinem; Öndeş, Baha
  • Applied Biochemistry and Biotechnology, Vol. 193, Issue 5
  • DOI: 10.1007/s12010-020-03476-7