Mimicking biological electron transport in sol-gel glass: photoinduced electron transfer from zinc cytochrome C to plastocyanin or cytochrome C mediated by mobile inorganic complexes.

Biomimetic studies of electron-transport chains are important for establishing the molecular mechanisms of long-range communications between proteins. We mimic these biological assemblies by encapsulating metalloproteins in sol-gel silica glass and letting mobile inorganic complexes shuttle electrons between the immobilized proteins. We present two examples of such rudimentary electron-transport chains. In both of them the immobilized electron donor is the zinc-substituted cytochrome c, Zncyt; the immobilized electron acceptor is either cupriplastocyanin, pc(II), or ferricytochrome c, cyt(III); and the mobile charge carrier Q/Q(-) is the redox couple FeEDTA(-)(/2)(-) or Ru(NH(3))(6)(3+/2+). The redox processes are photoinduced: Zncyt is excited by the laser pulse and converted to the triplet state, (3)Zncyt, which is a strong reducing agent. Visible absorption, circular dichroism, and electron paramagnetic resonance spectra of the metalloproteins show that encapsulation in sol-gel glass does not affect their intrinsic redox properties. The rigid silica glass spatially separates the proteins from each other. In this matrix, the electron-transfer reactions between (3)Zncyt and pc(II) and between (3)Zncyt and cyt(III), which occur fast in solution, are completely suppressed in the absence of a charge carrier Q/Q(-). The reactivity of FeEDTA(-) and Ru(NH(3))(6)(3+) (as quenchers Q of (3)Zncyt) is minimally affected by the interior of the sol-gel glass. In the glass, the second-order rate constants for the excited-state electron transfer, from (3)Zncyt to Q, are (8.9 +/- 0.6) x 10(6) and (8.0 +/- 2.4) x 10(6) M(-)(1) s(-)(1) for FeEDTA(-) and Ru(NH(3))(6)(3+), respectively. This reaction is followed by the ground-state back electron transfer, from Q(-) to Zncyt(+). In the "monoprotein" glasses Zncyt/Q, the respective second-order rate constants for this back electron-transfer reaction are (4.9 +/- 0.2) x 10(7) and (7.8 +/- 2.7) x 10(7) M(-)(1) s(-)(1). In the "diprotein" glasses Zncyt/Q/pc(II) and Zncyt/Q/cyt(III), containing also the acceptor protein pc(II) or cyt(III), Zncyt(+) decays on two time scales. The faster and major component of this decay is analogous to the only mode of the decay in the Zncyt/Q glasses and is a second-order process. Between 25 and 40% of the initially formed Zncyt(+), however, lives longer (k(slow) =1.1 +/- 0.2 s(-)(1)) and decays by a first-order process. We attribute the lengthening of the Zncyt(+) lifetime to a partial escape of the photogenerated Q(-) into the glass pores, where it reacts with the immobilized pc(II) or cyt(III). Indeed, the visible absorption spectra show the photoinduced reduction of pc(II) and cyt(III). Evidently, the small inorganic complexes, FeEDTA(-)(/2)(-) and Ru(NH(3))(6)(3+/2+), move through the glass pores, react with the encapsulated metalloproteins, and establish the interprotein electron transfer. Each interprotein reaction now occurs in two steps: a mobile charge carrier Q receives an electron from (3)Zncyt, and Q(-) then delivers an electron to pc(II) or cyt(III). Ultimately, the energy of visible light is converted to reducing equivalents for plastocyanin and cytochrome c. The sequential electron transfer described here resembles the events in a rudimentary electron-transport chain. Our findings demonstrate the promise of integrating proteins, with their optimally adjusted redox sites, in photocatalytic materials.