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Title: Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances

Abstract

Humic substances (HS) constitute a significant fraction of natural organic matter in terrestrial and aquatic environments and can act as terminal electron acceptors in anaerobic microbial respiration. Geobacter sulfurreducens has a remarkable respiratory versatility and can utilize the HS analog anthraquinone-2,6-disulfonate (AQDS) as a terminal electron acceptor or its reduced form (AH2QDS) as an electron donor. Previous studies set the triheme cytochrome PpcA as a key component for HS respiration in G. sulfurreducens, but the process is far from fully understood. In this work, NMR chemical shift perturbation measurements were used to map the interaction region between PpcA and AH2QDS, and to measure their binding affinity. The results showed that the AH2QDS binds reversibly to the more solvent exposed edge of PpcA heme IV. The NMR and visible spectroscopies coupled to redox measurements were used to determine the thermodynamic parameters of the PpcA:quinol complex. The higher reduction potential of heme IV (- 127 mV) compared to that of AH2QDS (- 184 mV) explains why the electron transfer is more favorable in the case of reduction of the cytochrome by the quinol. The clear evidence obtained for the formation of an electron transfer complex between AH2QDS and PpcA, combined with themore » fact that the protein also formed a redox complex with AQDS, revealed for the first time the bifunctional behavior of PpcA toward an analog of the HS. In conclusion, such behavior might confer selective advantage to G. sulfurreducens, which can utilize the HS in any redox state available in the environment for its metabolic needs.« less

Authors:
; ; ;
Publication Date:
Research Org.:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1328057
Alternate Identifier(s):
OSTI ID: 1339099
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Journal Article: Published Article
Journal Name:
Biochimica et Biophysica Acta - Bioenergetics
Additional Journal Information:
Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Volume: 1847 Journal Issue: 10; Journal ID: ISSN 0005-2728
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Electron transfer; Geobacter; Humics; Multiheme cytochromes; NMR

Citation Formats

Dantas, Joana M., Kokhan, Oleksandr, Pokkuluri, P. Raj, and Salgueiro, Carlos A. Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances. Netherlands: N. p., 2015. Web. doi:10.1016/j.bbabio.2015.06.004.
Dantas, Joana M., Kokhan, Oleksandr, Pokkuluri, P. Raj, & Salgueiro, Carlos A. Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances. Netherlands. https://doi.org/10.1016/j.bbabio.2015.06.004
Dantas, Joana M., Kokhan, Oleksandr, Pokkuluri, P. Raj, and Salgueiro, Carlos A. 2015. "Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances". Netherlands. https://doi.org/10.1016/j.bbabio.2015.06.004.
@article{osti_1328057,
title = {Molecular interaction studies revealed the bifunctional behavior of triheme cytochrome PpcA from Geobacter sulfurreducens toward the redox active analog of humic substances},
author = {Dantas, Joana M. and Kokhan, Oleksandr and Pokkuluri, P. Raj and Salgueiro, Carlos A.},
abstractNote = {Humic substances (HS) constitute a significant fraction of natural organic matter in terrestrial and aquatic environments and can act as terminal electron acceptors in anaerobic microbial respiration. Geobacter sulfurreducens has a remarkable respiratory versatility and can utilize the HS analog anthraquinone-2,6-disulfonate (AQDS) as a terminal electron acceptor or its reduced form (AH2QDS) as an electron donor. Previous studies set the triheme cytochrome PpcA as a key component for HS respiration in G. sulfurreducens, but the process is far from fully understood. In this work, NMR chemical shift perturbation measurements were used to map the interaction region between PpcA and AH2QDS, and to measure their binding affinity. The results showed that the AH2QDS binds reversibly to the more solvent exposed edge of PpcA heme IV. The NMR and visible spectroscopies coupled to redox measurements were used to determine the thermodynamic parameters of the PpcA:quinol complex. The higher reduction potential of heme IV (- 127 mV) compared to that of AH2QDS (- 184 mV) explains why the electron transfer is more favorable in the case of reduction of the cytochrome by the quinol. The clear evidence obtained for the formation of an electron transfer complex between AH2QDS and PpcA, combined with the fact that the protein also formed a redox complex with AQDS, revealed for the first time the bifunctional behavior of PpcA toward an analog of the HS. In conclusion, such behavior might confer selective advantage to G. sulfurreducens, which can utilize the HS in any redox state available in the environment for its metabolic needs.},
doi = {10.1016/j.bbabio.2015.06.004},
url = {https://www.osti.gov/biblio/1328057}, journal = {Biochimica et Biophysica Acta - Bioenergetics},
issn = {0005-2728},
number = 10,
volume = 1847,
place = {Netherlands},
year = {Thu Oct 01 00:00:00 EDT 2015},
month = {Thu Oct 01 00:00:00 EDT 2015}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at https://doi.org/10.1016/j.bbabio.2015.06.004

Citation Metrics:
Cited by: 12 works
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