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Sorption and Direct Electrochemistry of Mitochondrial Cytochrome C on Hematite Surfaces

Published online by Cambridge University Press:  01 January 2024

Nidhi Khare ,
Carrick M. Eggleston  and
David M. Lovelace
Nidhi Khare*
Affiliation:
Department of Geology and Geophysics, University of Wyoming, Laramie, Wyoming 82071, USA
Carrick M. Eggleston
Affiliation:
Department of Geology and Geophysics, University of Wyoming, Laramie, Wyoming 82071, USA
David M. Lovelace
Affiliation:
Department of Geology and Geophysics, University of Wyoming, Laramie, Wyoming 82071, USA
*
*E-mail address of corresponding author: [email protected]
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Abstract

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The interaction of cytochromes (heme proteins) with mineral surfaces is important from an environmental perspective (e.g. heavy metal remediation and reductive dehalogenation reactions), for designing biosensors and bioanalytical systems, and for emerging photovoltaic applications. In addition, the cytochrome studied here shares properties with some cytochromes from Fe-reducing bacteria and its general behavior sheds light on how other cytochromes might behave during Fe(III) reduction. The objectives of this study were to characterize the direct electrochemistry and sorption mechanism of horse heart ferricytochrome c (a mitochondrial cytochrome referred to as Hcc) on hematite surfaces as a function of pH, time of sorption and ionic strength. Hcc sorption on hematite mainly occurs between pH 8 and 10, the pH range in which hematite surfaces and Hcc are oppositely charged. Calculated net attractive forces correspond closely with the pH range of peak sorption, suggesting that sorption is mainly electrostatically controlled. Hcc sorption with ionic strength is consistent with this conclusion. The pH-dependent conformation of Hcc sorbed on hematite appears to be different from that in solution as indicated by UV-visible spectroscopy and its more negative reduction potential compared to native Hcc. Sorption kinetics were rapid and pH-independent across the pH range 3–10 with slow conformational changes occurring at >60 h. Our results suggest that the electrostatic attraction of the cytochrome towards the surface orient the cytochrome for favorable electron transfer between the heme group of the cytochrome and hematite.

Keywords

Cytochrome cFe OxideHematiteProteinSorption
Type
Research Article
Information
Clays and Clay Minerals , Volume 53 , Issue 6 , December 2005 , pp. 564 - 571
Copyright
Copyright © 2005, The Clay Minerals Society

References

Anderson, A.B. and Robertson, C.R., (1995) Absorption spectra indicate conformational alteration of myoglobin adsorbed on polymethylsiloxane Biophysical Journal 68 2091–2097 10.1016/S0006-3495(95)80388-7.CrossRefGoogle Scholar
Boffi, F. Bonincontro, S. Cinelli, A. Castellano, C. De Francesco, A. Delia Longa, S. Girasole, M. and Onori, G., (2001) pH dependent local structure of ferricytochrome c studied by X-ray absorption spectroscopy Biophysical Journal 80 1473–1479 10.1016/S0006-3495(01)76119-X.CrossRefGoogle ScholarPubMed
Bowden, E.F. Hawkridge, F.M. and Blount, H.N., (1984) Interfacial electrochemistry of cytochrome c at tin oxide, indium oxide, gold, and platinum electrodes Journal of Electroanalytical Chemistry 161 355–376 10.1016/S0022-0728(84)80193-X.CrossRefGoogle Scholar
Cao, D. He, P. and Hu, N., (2003) Electrochemical biosensors utilizing electron transfer in heme proteins immobilized on Fe3O4 nanoparticles Analyst 128 1268–1274 10.1039/B308242C.CrossRefGoogle ScholarPubMed
Castro, C.E. Wade, R.S. and Belser, N.O., (1985) Biodehalogenation: Reactions of cytochrome P-450 with polyhalomethanes Biochemistry 24 204–210 10.1021/bi00322a029.CrossRefGoogle ScholarPubMed
Chen, X. Ferrigno, R. Yang, J. and Whitesides, G.M., (2002) Redox properties of cytochrome c adsorbed on self-assembled monolayers: A probe for protein conformation and orientation Langmuir 18 7009–7015 10.1021/la0204794.CrossRefGoogle Scholar
Das, R. Kiley, P.J. Segal, M. Norville, J. Yu, A.A. Wang, L. Trammell, S.A. Reddick, L.E. Kumar, R. Stellacci, F. Lebedev, N. Schnur, J. Bruce, B.D. Zhang, S. and Baldo, M., (2004) Integration of photosynthetic protein molecular complexes in solid-state electronic devices Nano Letters 4 1079–1083 10.1021/nl049579f.CrossRefGoogle Scholar
Dick, L.A. Haes, A.J. and Van Duyne, R.P., (2000) Distance and orientation dependence of heterogeneous electron transfer: A surface-enhanced resonance Raman scattering study of cytochrome c bound to carboxylic acid terminated alkanethiols adsorbed on silver electrodes Journal of Physical Chemistry 104 11752–11762 10.1021/jp0029717.CrossRefGoogle Scholar
Fridman, V. Wollenberger, U. Bogdanovskaya, V. Lisdat, F. Ruzgas, T. Lindgren, A. Gorton, L. and Scheller, F.W., (2000) Biosensors and novel bioanalytical methods Biochemical Society Transactions 28 2 63–70 10.1042/bst0280063.CrossRefGoogle Scholar
Gorton, L. Lindgren, A. Larsson, T. Munteanu, F.D. Ruzzas, T. and Gazaryan, I., (1999) Direct electron transfer between heme containing enzymes and electrodes as basis for third generation biosensors Analytica Chimica Acta 400 103 91–108 10.1016/S0003-2670(99)00610-8.CrossRefGoogle Scholar
Kano, K. and Ikeda, T., (2000) Fundamentals and practices of mediated bioelectrocatalysis Analytical Sciences 16 10 1013–1021 10.2116/analsci.16.1013.CrossRefGoogle Scholar
Khare, N. Hesterberg, D. Beauchemin, S. and Wang, S.-L., (2004) XANES determination of adsorbed phosphate distribution between ferrihydrite and boehmite in mixtures Soil Science Society of America Journal 68 460–469 10.2136/sssaj2004.4600.CrossRefGoogle Scholar
Koutsoukos, P.G. Norde, W. and Lyklema, J., (1983) Protein adsorption on hematite (oc-Fe2O3) surfaces Journal of Colloid and Interface Science 95 385–396 10.1016/0021-9797(83)90198-4.CrossRefGoogle Scholar
Lojou, E. and Bianco, P., (2000) Membrane electrodes can modulate the electrochemical response of redox proteins—direct electrochemistry of cytochrome c Journal of Electroanalytical Chemistry 485 71–80 10.1016/S0022-0728(00)00102-9.CrossRefGoogle Scholar
Lojou, E. and Bianco, P., (2003) Quartz crystal microbalance and voltammetry monitoring for layer by layer assembly of cytochrome c3 and poly (ester sulfonic acid) films on gold and silver electrodes Journal of Electroanalytical Chemistry 557 37–47 10.1016/S0022-0728(03)00347-4.CrossRefGoogle Scholar
Lojou, E. Bianco, P. and Bruschi, M., (1998) Kinetic studies on the electron transfer between bacterial c-type cytochromes and metal oxides Journal of Electroanalytical Chemistry 452 167–177 10.1016/S0022-0728(98)00141-7.CrossRefGoogle Scholar
Millett, F. Durham, B., Scott, R.A. and Grant Mauk, A., (1996) Chemical modification of surface residues on cytochrome c. Cytochrome-c: A multidisciplinary Approach Sausalito, California University Science Books 573–591.Google Scholar
Neal, B.L. Asthagiri, D. Velev, O.D. Lenhoff, A.M. and Kaler, E.W., (1999) Why is the osmotic second virial coefficient related to protein crystallization? Journal of Crystal Growth 196 377–387 10.1016/S0022-0248(98)00855-0.CrossRefGoogle Scholar
Parks, G.A. and De Bruyn, P.L., (1962) The zero point of charge of oxides Journal of Physical Chemistry 66 967–973 10.1021/j100812a002.CrossRefGoogle Scholar
Peng, X. Huang, J. and Ji, L., (2000) The self aggregation of Chiral threonine-linked porphyrins and their Zn(II) complexes Chinese Science Bulletin 45 418–421 10.1007/BF02884941.CrossRefGoogle Scholar
Pinheiro, T.J.T., (1994) The interaction of horse heart cytochrome c with phospholipid bilayers. Structural and dynamic effects Biochimie 76 489–500 10.1016/0300-9084(94)90173-2.CrossRefGoogle ScholarPubMed
Saliez, Y. Bianco, P. and Lojou, E., (2000) Electrochemical behavior of c-type cytochromes at clay-modified carbon electrodes: A model for the interaction between proteins and soils Journal of Electroanalytical Chemistry 493 37–49 10.1016/S0022-0728(00)00280-1.CrossRefGoogle Scholar
Santos, J.H. Matsuda, N. Qi, Z.-M. Yoshida, T. Takatsu, A. and Kato, K., (2003) Adsorption behavior of cytochrome c, myoglobin and haemoglobin in a quartz surface probed using slab optical waveguide (SOWG) spectroscopy Analytical Sciences 19 199–204 10.2116/analsci.19.199.CrossRefGoogle Scholar
Schudel, M. Behrens, S.H. Holthoff, H. Kretzschmar, R. and Borkovec, M., (1997) Absolute aggregation rate constants of hematite particles in aqueous suspensions: A comparison of two different surface morphologies Journal of Colloid and Interface Science 196 241–253 10.1006/jcis.1997.5207.CrossRefGoogle ScholarPubMed
Shanker, R. and Atkins, W.M., (1996) Luciferase-dependent, cytochrome P-450-catalyzed dehalogenation in genetically engineered Pseudomonas Biotechnology Progress 12 474–479 10.1021/bp9600389.CrossRefGoogle ScholarPubMed
Sugimoto, T. Muramatsu, A. Sakata, K. and Shindo, D., (1993) Characterization of hematite particles of different shapes Journal of Colloid and Interface Science 158 420–428 10.1006/jcis.1993.1274.CrossRefGoogle Scholar
Stumm, W. and Morgan, J.J., (1996) Aquatic Chemistry 3rd edition New York John Wiley & Sons, Inc..Google Scholar
Theorell, H. and Akesson, A., (1941) Studies on cytochrome c. III. Titration curves Journal of the American Chemical Society 63 1818–1820 10.1021/ja01852a007.CrossRefGoogle Scholar
Topoglidis, E. Campbell, C.J. Palomares, E. and Durrant, J.R., (2002) Photoelectrochemical study of Zn cytochrome-c immobilized on a nanoporous metal oxide electrode Chemical Communications 2002 1518–1519 10.1039/b203448d.CrossRefGoogle Scholar
Vilker, V.L. Uyeno, G.P. and McMillan, W.G., (1981) Solvent effect on the dispersion (Hamaker-London) coefficient from third-order perturbation theory Journal of Physical Chemistry 85 2013–2021 10.1021/j150614a012.CrossRefGoogle Scholar
Whitford, D. Concar, D.W. and Williams, R.J.P., (1991) The promotion of self-association of horse-heart cytochrome c by hexametaphosphate anions European Journal of Biochemistry 199 561–568 10.1111/j.1432-1033.1991.tb16155.x.CrossRefGoogle ScholarPubMed
Wirtz, M. Klucik, J. and Rivera, M., (2000) Ferredoxin mediated electrocatalytic dehalogenation of haloalkanes by cytochrome P450cam Journal of the American Chemical Society 122 6 1047–1056 10.1021/ja993648o.CrossRefGoogle Scholar
Yeh, P. and Kuwana, T., (1977) Reversible electrode reaction of cytochrome c Chemistry Letters 1977 1145–1148 10.1246/cl.1977.1145.CrossRefGoogle Scholar