journal article·2014-06

Proton switch for modulating oxygen reduction by a copper electrocatalyst embedded in a hybrid bilayer membrane

Christopher J. Barile, Edmund C. M. Tse, Ying Li, Thomas B. Sobyra, Steven C. Zimmerman, Ali Hosseini, Andrew A. Gewirth

Nature Materials· Volume 13· Issue 6
Publisher page

Abstract

Molecular switches gate many fundamental processes in natural and artificial systems. Here, we report the development of an electrochemical platform in which a proton carrier switches the activity of a catalyst. By incorporating an alkyl phosphate in the lipid layer of a hybrid bilayer membrane, we regulate proton transport to a Cu-based molecular oxygen reduction reaction catalyst. To construct this hybrid bilayer membrane system, we prepare an example of a synthetic Cu oxygen reduction reaction catalyst that forms a self-assembled monolayer on Au surfaces. We then embed this Cu catalyst inside a hybrid bilayer membrane by depositing a monolayer of lipid on the self-assembled monolayer. We envisage that this electrochemical system can give a unique mechanistic insight not only into the oxygen reduction reaction, but into proton-coupled electron transfer in general.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Electrocatalysts for Energy Conversion · Molecular Junctions and Nanostructures · Fuel Cells and Related Materials

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (46)

Show source-provided references
1. Browne, W. R. & Feringa, B. L. Making molecular machines work. Nature Nanotech. 1, 25–35 (2006).10.1038/nnano.2006.45 ↗
2. Balzani, V., Credi, A., Raymo, F. M. & Stoddart, J. F. Artificial molecular machines. Angew. Chem. Int. Ed. 39, 3348–3391 (2000).10.1002/1521-3773(20001002)39:19<3348::AID-ANIE3348>3.0.CO;2-X ↗
3. Hirjibehedin, C. F. et al. Large magnetic anisotropy of a single atomic spin embedded in a surface molecular network. Science 317, 1199–1203 (2007).10.1126/science.1146110 ↗
4. Fuentes, N. et al. Organic-based molecular switches for molecular electronics. Nanoscale 3, 4003–4014 (2011).10.1039/c1nr10536a ↗
5. Alberts, B. et al. Molecular Biology of the Cell 4th edn (Garland Science, 2002).
6. Von Lintig, J., Kiser, P. D., Golczak, M. & Palczewski, K. The biochemical and structural basis for trans-to-cis isomerization of retinoids in the chemistry of vision. Trends Biochem. Sci. 35, 400–410 (2010).10.1016/j.tibs.2010.01.005 ↗
7. Donaldson, J. & Segev, N. Trafficking Inside Cells: Pathways, Mechanisms and Regulation (Landes Bioscience and Springer Science, 2009).
8. Lee, H. J., Gennis, R. B. & Ädelroth, P. Entrance of the proton pathway in cbb3-type heme-copper oxidases. Proc. Natl Acad. Sci. USA 108, 17661–17666 (2011).10.1073/pnas.1107543108 ↗
9. Mayer, J. M. Proton-coupled electron transfer: A reaction chemist’s view. Annu. Rev. Phys. Chem. 55, 363–390 (2004).10.1146/annurev.physchem.55.091602.094446 ↗
10. Chen, Z., Vannucci, A. K., Concepcion, J. J., Jurss, J. W. & Meyer, T. J. Proton-coupled electron transfer at modified electrodes by multiple pathways. Proc. Natl Acad. Sci. USA 108, E1461–E1469 (2011).10.1073/pnas.1115769108 ↗
11. Huynh, M. H. V. & Meyer, T. J. Proton-coupled electron transfer. Chem. Rev. 107, 5004–5064 (2007).10.1021/cr0500030 ↗
12. Wenger, O. S. Proton-coupled electron transfer with photoexcited metal complexes. Acc. Chem. Res. 46, 1517–1526 (2013).10.1021/ar300289x ↗
13. Thorseth, M. A., Tornow, C. E., Tse, E. C. M. & Gewirth, A. A. Cu complexes that catalyze the oxygen reduction reaction. Coord. Chem. Rev. 257, 130–139 (2013).10.1016/j.ccr.2012.03.033 ↗
14. Boulatov, R., Collman, J. P., Shiryaeva, I. M. & Sunderland, C. J. Functional analogues of the dioxygen reduction site in cytochrome oxidase: mechanistic aspects and possible effects of CuB . J. Am. Chem. Soc. 124, 11923–11935 (2002).10.1021/ja026179q ↗
15. Thorseth, M. A., Letko, C. S., Rauchfuss, T. B. & Gewirth, A. A. Dioxygen and hydrogen peroxide reduction with hemocyanin model complexes. Inorg. Chem. 50, 6158–6162 (2011).10.1021/ic200386d ↗
16. Oberst, J. L., Thorum, M. S. & Gewirth, A. A. Effect of pH and azide on the oxygen reduction reaction with a pyrolyzed Fe phthalocyanine catalyst. J. Phys. Chem. C 116, 25257–25261 (2012).10.1021/jp309707b ↗
17. Rosenthal, J. & Nocera, D. G. Role of proton-coupled electron transfer in O–O bond activation. Acc. Chem. Res. 40, 543–553 (2007).10.1021/ar7000638 ↗
18. Chng, L. L., Chang, C. J. & Nocera, D. G. Catalytic O–O activation chemistry mediated by iron hangman porphyrins with a wide range of proton-donating abilities. Org. Lett. 5, 2421–2424 (2003).10.1021/ol034581j ↗
19. Thorseth, M. A., Letko, C. S., Tse, E. C. M., Rauchfuss, T. B. & Gewirth, A. A. Ligand effects on the overpotential for dioxygen reduction by tris(2-pyridylmethyl)amine derivatives. Inorg. Chem. 52, 628–634 (2013).10.1021/ic301656x ↗
20. Hosseini, A. et al. Hybrid bilayer membrane: A platform to study the role of proton flux on the efficiency of oxygen reduction by a molecular electrocatalyst. J. Am. Chem. Soc. 133, 11100–11102 (2001).10.1021/ja204418j ↗
21. Plant, A. L. Self-assembled phospholipid/alkanethiol biomimetic bilayers on gold. Langmuir 9, 2764–2767 (1993).10.1021/la00035a004 ↗
22. Plant, A. L. Supported hybrid bilayer membranes as rugged cell membrane mimics. Langmuir 15, 5128–5135 (1999).10.1021/la981662t ↗
23. Twardowski, M. & Nuzzo, R. G. Molecular recognition at model organic interfaces: Electrochemical discrimination using self-assembled monolayers (SAMs) modified via the fusion of phospholipid vesicles. Langmuir 19, 9781–9791 (2003).10.1021/la0349018 ↗
24. Twardowski, M. & Nuzzo, R. G. Phase dependent electrochemical properties of polar self-assembled monolayers (SAMs) modified via the fusion of mixed phospholipid vesicles. Langmuir 20, 175–180 (2004).10.1021/la035074d ↗
25. Thorum, M. S., Yadav, J. & Gewirth, A. A. Oxygen reduction activity of a copper complex of 3,5-diamino-1,2,4-triazole supported on carbon black. Angew. Chem. Int. Ed. 48, 165–167 (2009).10.1002/anie.200803554 ↗
26. Devaraj, N. K., Decreau, R. A., Ebina, W., Collman, J. P. & Chidsey, C. E. D. Rate of interfacial electron transfer through the 1,2,3-triazole linkage. J. Phys. Chem. B 110, 15955–15962 (2006).10.1021/jp057416p ↗
27. Inman, C. E., Reed, S. M. & Hutchison, J. E. In situ deprotection and assembly of s-tritylalkanethiols on gold yields monolayers comparable to those prepared directly from alkanethiols. Langmuir 20, 9144–9150 (2004).10.1021/la049627b ↗
28. Ermakova, T. G. et al. Polarographic reduction of 1-substituted 1,2,4-triazoles. Chem. Heterocyc. Compd. 16, 313–315 (1980).10.1007/BF02401735 ↗
29. Hosseini, A. et al. Ferrocene embedded in an electrode-supported hybrid lipid bilayer membrane: A model system for electrocatalysis in a biomimetic environment. Langmuir 26, 17674–17678 (2010).10.1021/la1029118 ↗
30. Rowe, G. K. & Creager, S. E. Interfacial solvation and double-layer effects on redox reactions in organized assemblies. J. Phys. Chem. 98, 5500–5507 (1994).10.1021/j100072a017 ↗
31. Subczynski, W. K. & Hyde, J. S. Concentration of oxygen in lipid bilayers using a spin-label method. Biophys. J. 41, 283–286 (1983).10.1016/S0006-3495(83)84439-7 ↗
32. Windrem, D. A. & Plachy, W. Z. The diffusion-solubility of oxygen in lipid bilayers. Biochim. Biophys. Acta 600, 655–665 (1980).10.1016/0005-2736(80)90469-1 ↗
33. Chang, P. & Wilke, C. R. Some measurements of diffusion in liquids. J. Phys. Chem. 59, 592–596 (1955).10.1021/j150529a005 ↗
34. Jain, M. K. Introduction to Biological Membranes 2nd edn (Wiley, 1988).
35. Collman, J. P. et al. A cytochrome c oxidase model catalyzes oxygen to water reduction under rate-limiting electron flux. Science 315, 1565–1568 (2007).10.1126/science.1135844 ↗
36. Collman, J. P. et al. Role of a distal pocket in the catalytic O2 reduction by cytochrome c oxidase models immobilized on interdigitated array electrodes. Proc. Natl Acad. Sci. USA 106, 7320–7323 (2009).10.1073/pnas.0902285106 ↗
37. Srivastava, A., Singh, S. & Krishnamoorthy, G. Rapid transport of protons across membranes by aliphatic amines and acids. J. Phys. Chem. 99, 11302–11305 (1995).10.1021/j100029a002 ↗
38. Schönfeld, P., Schild, L. & Kunz, W. Long-chain fatty acids act as protonophoric uncouplers of oxidative phosphorylation in rat liver mitochondria. Biochim. Biophys. Acta 977, 266–272 (1989).10.1016/S0005-2728(89)80080-5 ↗
39. McConnell, H. M. & Kornberg, R. D. Inside–outside transitions of phospholipids in vesicle membranes. Biochemistry 10, 1111–1120 (1971).10.1021/bi00783a003 ↗
40. Palermo, E. F., Lee, D-K., Ramamoorthy, A. & Kuroda, K. Role of cationic group structure in membrane binding and disruption by amphiphilic copolymers. J. Phys. Chem. B 115, 366–375 (2010).10.1021/jp1083357 ↗
41. Albrecht, O., Gruler, H. & Sackmann, E. Polymorphism of phospholipid monolayers. J. Phys. France 39, 301–313 (1978).10.1051/jphys:01978003903030100 ↗
42. John, K., Schreiber, S., Kubelt, J., Herrmann, A. & Müller, P. Transbilayer movement of phospholipids at the main phase transition of lipid membranes: Implications for rapid flip–flop in biological membranes. Biophys. J. 83, 3315–3323 (2002).10.1016/S0006-3495(02)75332-0 ↗
43. Han, X., Wang, L., Qi, B., Yang, X. & Wang, E. A strategy for constructing a hybrid bilayer membrane based on a carbon substrate. Anal. Chem. 75, 6566–6570 (2003).10.1021/ac034592q ↗
44. Mercado, F. V., Maggio, R. & Wilke, N. Phase diagram of mixed monolayers of stearic acid and dimyristoylphosphatidylcholine. Effect of the acid ionization. Chem. Phys. Lipids 164, 386–392 (2011).10.1016/j.chemphyslip.2011.05.004 ↗
45. Mercado, F. V., Maggio, R. & Wilke, N. Modulation of the domain topography of biphasic monolayers of stearic acid and dimyristoyl phosphatidylcholine. Chem. Phys. Lipids 165, 232–237 (2012).10.1016/j.chemphyslip.2012.01.003 ↗
46. Gong, K., Du, F., Xia, Z., Durstock, M. & Dai, L. Nitrogen-doped carbon nanotube arrays with high electrocatalytic activity for oxygen reduction. Science 323, 760–764 (2009).10.1126/science.1168049 ↗