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Title: Electron Paramagnetic Resonance Characterization of the Triheme Cytochrome from Geobacter sulfurreducens

Abstract

Periplasmic cytochrome A (PpcA) is a representative of a broad class of multiheme cytochromes functioning as protein “nanowires” for storage and extracellular transfer of multiple electrons in the δ-proteobacterium Geobacter sulfurreducens. PpcA contains three bis-His coordinated hemes held in a spatial arrangement that is highly conserved among the multiheme cytochromes c3 and c7 families, carries low potential hemes, and is notable for having one of the lowest number of amino acids utilized to maintain a characteristic protein fold and site-specific heme function. Low temperature X-band electron paramagnetic resonance (EPR) spectroscopy has been used to characterize the electronic configuration of the Fe(III) and the ligation mode for each heme. The three sets of EPR signals are assigned to individual hemes in the three-dimensional crystal structure. The relative energy levels of the Fe(III) 3d orbitals for individual hemes were estimated from the principal g-values. The observed g-tensor anisotropy was used as a probe of electronic structure of each heme, and differences were determined by specifics of axial ligation. To ensure unambiguous assignment of highly anisotropic low-spin (HALS) signal to individual hemes, EPR analyses of iron atom electronic configurations have been supplemented with investigation of porphyrin macrocycles by one-dimensional 1H NMR chemical shiftmore » patterns for the methyl substituents. In conclusion, within optimized geometry of hemes in PpcA, the magnetic interactions between hemes were found to be minimal, similar to the c3 family of tetraheme cytochromes.« less

Authors:
ORCiD logo [1]; ORCiD logo [1];  [2];  [1];  [1]
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  1. Argonne National Lab. (ANL), Argonne, IL (United States). Chemical Sciences and Engineering Division
  2. Argonne National Lab. (ANL), Argonne, IL (United States). Biosciences Division
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, and Biosciences Division
OSTI Identifier:
1427531
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 57; Journal Issue: 11; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 1H NMR; Geobacter sulfurreducens; Periplasmic cytochrome A; PpcA; X-band EPR; heme coordination; triheme cytochrome

Citation Formats

Ponomarenko, Nina, Niklas, Jens, Pokkuluri, P. Raj, Poluektov, Oleg, and Tiede, David M. Electron Paramagnetic Resonance Characterization of the Triheme Cytochrome from Geobacter sulfurreducens. United States: N. p., 2018. Web. doi:10.1021/acs.biochem.7b00917.
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Ponomarenko, Nina, Niklas, Jens, Pokkuluri, P. Raj, Poluektov, Oleg, & Tiede, David M. Electron Paramagnetic Resonance Characterization of the Triheme Cytochrome from Geobacter sulfurreducens. United States. https://doi.org/10.1021/acs.biochem.7b00917
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Ponomarenko, Nina, Niklas, Jens, Pokkuluri, P. Raj, Poluektov, Oleg, and Tiede, David M. Wed . "Electron Paramagnetic Resonance Characterization of the Triheme Cytochrome from Geobacter sulfurreducens". United States. https://doi.org/10.1021/acs.biochem.7b00917. https://www.osti.gov/servlets/purl/1427531.
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@article{osti_1427531,
title = {Electron Paramagnetic Resonance Characterization of the Triheme Cytochrome from Geobacter sulfurreducens},
author = {Ponomarenko, Nina and Niklas, Jens and Pokkuluri, P. Raj and Poluektov, Oleg and Tiede, David M.},
abstractNote = {Periplasmic cytochrome A (PpcA) is a representative of a broad class of multiheme cytochromes functioning as protein “nanowires” for storage and extracellular transfer of multiple electrons in the δ-proteobacterium Geobacter sulfurreducens. PpcA contains three bis-His coordinated hemes held in a spatial arrangement that is highly conserved among the multiheme cytochromes c3 and c7 families, carries low potential hemes, and is notable for having one of the lowest number of amino acids utilized to maintain a characteristic protein fold and site-specific heme function. Low temperature X-band electron paramagnetic resonance (EPR) spectroscopy has been used to characterize the electronic configuration of the Fe(III) and the ligation mode for each heme. The three sets of EPR signals are assigned to individual hemes in the three-dimensional crystal structure. The relative energy levels of the Fe(III) 3d orbitals for individual hemes were estimated from the principal g-values. The observed g-tensor anisotropy was used as a probe of electronic structure of each heme, and differences were determined by specifics of axial ligation. To ensure unambiguous assignment of highly anisotropic low-spin (HALS) signal to individual hemes, EPR analyses of iron atom electronic configurations have been supplemented with investigation of porphyrin macrocycles by one-dimensional 1H NMR chemical shift patterns for the methyl substituents. In conclusion, within optimized geometry of hemes in PpcA, the magnetic interactions between hemes were found to be minimal, similar to the c3 family of tetraheme cytochromes.},
doi = {10.1021/acs.biochem.7b00917},
journal = {Biochemistry},
number = 11,
volume = 57,
place = {United States},
year = {Wed Jan 03 00:00:00 EST 2018},
month = {Wed Jan 03 00:00:00 EST 2018}
}
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https://doi.org/10.1021/acs.biochem.7b00917
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Figures / Tables:

Figure 1. Figure 1.: Ribbon representation of the PpcA cytochrome from G. sulfurreducens. The ribbon is colored in the range from blue (N terminus) to red (C terminus). The three heme groups are designated by Roman numerals according nomenclature common with tetraheme c3 cytochromes to account for the order of attachment tomore » the polypeptide chain. The inset on the left shows the heme diagram with the IUPAC nomenclature for identifying principle axes system and geometric parameters determining orientation angle Φ and interligand angle β used in this study. When looking at the heme from the sixth coordination site, the heme substituents are arranged in a clockwise order with increasing numbers corresponding to β-positions of the pyrrole rings. In particular, methyl groups are substituents at 2, 7, 12, 18 positions. Carbons with the implied numbers 5, 10, 15 and 20 located at generic meso-positions. The X axis goes through nitrogen 4 atoms N2 and N4, Y axis through N1 and N3 of corresponding pyrrole rings. The Z axis is aligned along the normal to the heme plane. The orientation angle Φ is measured from the X axis in counterclockwise direction to and past the Y axis until the average between the two histidine ligands positions. The interligand angle β is a dihedral angle between imidazole planes of histidine ligands.« less
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