Surface-induced intramolecular electron transfer in multi-centre redox metalloproteins: The di-haem protein cytochrome c4 in homogeneous solution and at electrochemical surfaces

Intramolecular electron transfer (ET) between transition metal centres is a core feature of biological ET and redox enzyme function. The number of microscopic redox potentials and ET rate constants is, however, mostly prohibitive for experimental mapping, but two-centre proteins offer simple enough communication networks for complete mapping to be within reach.

At the same time, multi-centre redox proteins operate in a membrane environment where conformational dynamics and ET patterns are quite different from the conditions in a homogeneous solution. The bacterial respiratory di-haem protein Pseudomonas stutzeri cytochrome c(4) offers a prototype target for environmental gating of intra-haem ET.

ET between P. stutzeri cyt c(4) and small molecular reaction partners in solution appears completely dominated by intermolecular ET of each haem group/protein domain, with no competing intra-haem ET, for which accompanying propionate-mediated proton transfer is a further barrier. The protein can, however, be immobilized on single-crystal, modified Au(111) electrode surfaces with either the low-potential N terminal or the high-potential C terminal domain facing the surface, clearly with fast intramolecular ET as a key feature in the electrochemical two-ET process.

This dual behaviour suggests a pattern for multi-centre redox metalloprotein function. In a homogeneous solution, which is not the natural environment of cyt c(4), the two haem group domains operate largely independently with conformations prohibitive for intramolecular ET. Binding to a membrane or electrochemical surface, however, triggers conformational opening of intramolecular ET channels.

The haem group orientation in P. stutzeri cyt c(4) is finally noted to offer a case for orientation dependent electronic rectification between a substrate and a tip in electrochemical in situ scanning tunnelling microscopy or nanoscale electrode configurations.