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 »
- Authors:
-
- Argonne National Lab. (ANL), Argonne, IL (United States). Chemical Sciences and Engineering Division
- 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:
- Journal Article: 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.
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
Ponomarenko, Nina, Niklas, Jens, Pokkuluri, P. Raj, Poluektov, Oleg, and Tiede, David M. 2018.
"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.
@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},
url = {https://www.osti.gov/biblio/1427531},
journal = {Biochemistry},
issn = {0006-2960},
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}
}
Web of Science
Figures / Tables:
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Works referencing / citing this record:
Examination of abiotic cofactor assembly in photosynthetic biomimetics: site-specific stereoselectivity in the conjugation of a ruthenium(II) tris(bipyridine) photosensitizer to a multi-heme protein
journal, January 2020
- Ponomarenko, Nina S.; Kokhan, Oleksandr; Pokkuluri, Phani R.
- Photosynthesis Research, Vol. 143, Issue 2