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Title: One Electron Multiple Proton Transfer in Model Organic Donor–Acceptor Systems: Implications for High-Frequency EPR

Abstract

EPR spectroscopy is an important spectroscopic method for identification and characterization of radical species involved in many biological reactions. The tyrosyl radical is one of the most studied amino acid radical intermediates in biology. Often in conjunction with histidine residues, it is involved in many fundamental biological electron and proton transfer processes, such as in the water oxidation in photosystem II. As biological processes are typically extremely complicated and hard to control, molecular bio-mimetic model complexes are often used to clarify the mechanisms of the biological reactions. In this work, we present theoretical calculations to investigate the sensitivity of magnetic resonance parameters to proton-coupled electron transfer events, as well as conformational substates of the molecular constructs which mimic the tyrosine-histidine (Tyr-His) pairs found in a large variety of proteins. Upon oxidation of the phenol, the Tyr analog, these complexes can perform not only one-electron one-proton transfer (EPT), but also one-electron two-proton transfers (E2PT). It is shown that in aprotic environment the gX-components of the electronicg-tensor are extremely sensitive to the first proton transfer from the phenoxyl oxygen to the imidazole nitrogen (EPT product), leading to a significant increase of the gX-value of up to 0.003, but are not sensitive tomore » the second proton transfer (E2PT). In the latter case, the change of the gX-value is much smaller (ca. 0.0001), which is too small to be distinguished even by high-frequency EPR. The 14N hyperfine values are also too similar to allow differentiation between the different protonation states in EPT and E2PT. The magnetic resonance parameters were also calculated as a function of the rotation angles around single bonds. It was demonstrated that rotation of the phenoxyl group results in large positive changes (> 0.001) in the gX-values. Analysis of the data reveals that the main source of these changes is related to the strength of the H-bond between phenoxyl oxygen and the proton(s) on N1 and N2 positions of the imidazole.« less

Authors:
 [1]; ORCiD logo [2];  [1];  [3];  [3];  [3]; ORCiD logo [2]
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  1. Chicago State Univ., IL (United States)
  2. Argonne National Lab. (ANL), Argonne, IL (United States)
  3. Arizona State Univ., Tempe, AZ (United States)
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division; National Institutes of Health (NIH)
OSTI Identifier:
1756649
Grant/Contract Number:  
AC02-06CH11357; FG02-03ER15393
Resource Type:
Accepted Manuscript
Journal Name:
Applied Magnetic Resonance
Additional Journal Information:
Journal Volume: 51; Journal Issue: 9-10; Journal ID: ISSN 0937-9347
Publisher:
Springer Nature
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; EPR; Photosynthesis; donor-acceptor

Citation Formats

Mardis, Kristy L., Niklas, Jens, Omodayo, Harriet, Odella, Emmanuel, Moore, Thomas A., Moore, Ana L., and Poluektov, Oleg G. One Electron Multiple Proton Transfer in Model Organic Donor–Acceptor Systems: Implications for High-Frequency EPR. United States: N. p., 2020. Web. doi:10.1007/s00723-020-01252-8.
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Mardis, Kristy L., Niklas, Jens, Omodayo, Harriet, Odella, Emmanuel, Moore, Thomas A., Moore, Ana L., & Poluektov, Oleg G. One Electron Multiple Proton Transfer in Model Organic Donor–Acceptor Systems: Implications for High-Frequency EPR. United States. https://doi.org/10.1007/s00723-020-01252-8
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Mardis, Kristy L., Niklas, Jens, Omodayo, Harriet, Odella, Emmanuel, Moore, Thomas A., Moore, Ana L., and Poluektov, Oleg G. Thu . "One Electron Multiple Proton Transfer in Model Organic Donor–Acceptor Systems: Implications for High-Frequency EPR". United States. https://doi.org/10.1007/s00723-020-01252-8. https://www.osti.gov/servlets/purl/1756649.
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@article{osti_1756649,
title = {One Electron Multiple Proton Transfer in Model Organic Donor–Acceptor Systems: Implications for High-Frequency EPR},
author = {Mardis, Kristy L. and Niklas, Jens and Omodayo, Harriet and Odella, Emmanuel and Moore, Thomas A. and Moore, Ana L. and Poluektov, Oleg G.},
abstractNote = {EPR spectroscopy is an important spectroscopic method for identification and characterization of radical species involved in many biological reactions. The tyrosyl radical is one of the most studied amino acid radical intermediates in biology. Often in conjunction with histidine residues, it is involved in many fundamental biological electron and proton transfer processes, such as in the water oxidation in photosystem II. As biological processes are typically extremely complicated and hard to control, molecular bio-mimetic model complexes are often used to clarify the mechanisms of the biological reactions. In this work, we present theoretical calculations to investigate the sensitivity of magnetic resonance parameters to proton-coupled electron transfer events, as well as conformational substates of the molecular constructs which mimic the tyrosine-histidine (Tyr-His) pairs found in a large variety of proteins. Upon oxidation of the phenol, the Tyr analog, these complexes can perform not only one-electron one-proton transfer (EPT), but also one-electron two-proton transfers (E2PT). It is shown that in aprotic environment the gX-components of the electronicg-tensor are extremely sensitive to the first proton transfer from the phenoxyl oxygen to the imidazole nitrogen (EPT product), leading to a significant increase of the gX-value of up to 0.003, but are not sensitive to the second proton transfer (E2PT). In the latter case, the change of the gX-value is much smaller (ca. 0.0001), which is too small to be distinguished even by high-frequency EPR. The 14N hyperfine values are also too similar to allow differentiation between the different protonation states in EPT and E2PT. The magnetic resonance parameters were also calculated as a function of the rotation angles around single bonds. It was demonstrated that rotation of the phenoxyl group results in large positive changes (> 0.001) in the gX-values. Analysis of the data reveals that the main source of these changes is related to the strength of the H-bond between phenoxyl oxygen and the proton(s) on N1 and N2 positions of the imidazole.},
doi = {10.1007/s00723-020-01252-8},
journal = {Applied Magnetic Resonance},
number = 9-10,
volume = 51,
place = {United States},
year = {Thu Oct 01 00:00:00 EDT 2020},
month = {Thu Oct 01 00:00:00 EDT 2020}
}
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