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A Comparative Multi-Frequency EPR Study of Dipolar Interaction in Tetra-Heme Cytochromes

Distances between Fe ions in multiheme cytochromes are sufficiently short to make the intramolecular dipole-dipole interaction between hemes probable. In the analysis of EPR data from cytochromes, this interaction has thus far been ignored under the assumption that spectra are the simple sum of non-...

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Autores principales: Hagen, Wilfred R., Louro, Ricardo O.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10454114/
https://www.ncbi.nlm.nih.gov/pubmed/37628894
http://dx.doi.org/10.3390/ijms241612713
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author Hagen, Wilfred R.
Louro, Ricardo O.
author_facet Hagen, Wilfred R.
Louro, Ricardo O.
author_sort Hagen, Wilfred R.
collection PubMed
description Distances between Fe ions in multiheme cytochromes are sufficiently short to make the intramolecular dipole-dipole interaction between hemes probable. In the analysis of EPR data from cytochromes, this interaction has thus far been ignored under the assumption that spectra are the simple sum of non-interacting components. Here, we use a recently developed low-frequency broadband EPR spectrometer to establish the extent of dipolar interaction in the example cytochromes, characterize its spectral signatures, and identify present limitations in the analysis. Broadband EPR spectra of Shewanella oneidensis MR-1 small tetraheme cytochrome (STC) have been collected over the frequency range of 0.45 to 13.11 GHz, and they have been compared to similar data from Desulfovibrio vulgaris Hildenborough cytochrome c(3). The two cases are representative examples of two very different heme topologies and corresponding electron-transfer properties in tetraheme proteins. While in cytochrome c(3), the six Fe-Fe distances can be sorted into two well-separated groups, those in STC are diffuse. Since the onset of dipolar interaction between Fe-Fe pairs is already observed in the X-band, the g values are determined in the simulation of the 13.11 GHz spectrum. Low-frequency spectra are analyzed with the inclusion of dipolar interaction based on available structural data on mutual distances and orientations between all hemes. In this procedure, all 24 possible assignments of individual heme spectra to heme topologies are sampled. The 24 configurations can be reduced to a few, but inspection falls short of a unique assignment, due to a remaining lack of understanding of the fine details of these complex spectra. In general, the EPR analysis suggests the four-heme system in c(3) to be more rigid than that in STC, which is proposed to be related to different physiological roles in electron transfer.
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spelling pubmed-104541142023-08-26 A Comparative Multi-Frequency EPR Study of Dipolar Interaction in Tetra-Heme Cytochromes Hagen, Wilfred R. Louro, Ricardo O. Int J Mol Sci Article Distances between Fe ions in multiheme cytochromes are sufficiently short to make the intramolecular dipole-dipole interaction between hemes probable. In the analysis of EPR data from cytochromes, this interaction has thus far been ignored under the assumption that spectra are the simple sum of non-interacting components. Here, we use a recently developed low-frequency broadband EPR spectrometer to establish the extent of dipolar interaction in the example cytochromes, characterize its spectral signatures, and identify present limitations in the analysis. Broadband EPR spectra of Shewanella oneidensis MR-1 small tetraheme cytochrome (STC) have been collected over the frequency range of 0.45 to 13.11 GHz, and they have been compared to similar data from Desulfovibrio vulgaris Hildenborough cytochrome c(3). The two cases are representative examples of two very different heme topologies and corresponding electron-transfer properties in tetraheme proteins. While in cytochrome c(3), the six Fe-Fe distances can be sorted into two well-separated groups, those in STC are diffuse. Since the onset of dipolar interaction between Fe-Fe pairs is already observed in the X-band, the g values are determined in the simulation of the 13.11 GHz spectrum. Low-frequency spectra are analyzed with the inclusion of dipolar interaction based on available structural data on mutual distances and orientations between all hemes. In this procedure, all 24 possible assignments of individual heme spectra to heme topologies are sampled. The 24 configurations can be reduced to a few, but inspection falls short of a unique assignment, due to a remaining lack of understanding of the fine details of these complex spectra. In general, the EPR analysis suggests the four-heme system in c(3) to be more rigid than that in STC, which is proposed to be related to different physiological roles in electron transfer. MDPI 2023-08-12 /pmc/articles/PMC10454114/ /pubmed/37628894 http://dx.doi.org/10.3390/ijms241612713 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Hagen, Wilfred R.
Louro, Ricardo O.
A Comparative Multi-Frequency EPR Study of Dipolar Interaction in Tetra-Heme Cytochromes
title A Comparative Multi-Frequency EPR Study of Dipolar Interaction in Tetra-Heme Cytochromes
title_full A Comparative Multi-Frequency EPR Study of Dipolar Interaction in Tetra-Heme Cytochromes
title_fullStr A Comparative Multi-Frequency EPR Study of Dipolar Interaction in Tetra-Heme Cytochromes
title_full_unstemmed A Comparative Multi-Frequency EPR Study of Dipolar Interaction in Tetra-Heme Cytochromes
title_short A Comparative Multi-Frequency EPR Study of Dipolar Interaction in Tetra-Heme Cytochromes
title_sort comparative multi-frequency epr study of dipolar interaction in tetra-heme cytochromes
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10454114/
https://www.ncbi.nlm.nih.gov/pubmed/37628894
http://dx.doi.org/10.3390/ijms241612713
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