Competition between intra-protein charge recombination and electron transfer outside photosystem I complexes used for photovoltaic applications

Abstract

Photosystem I (PSI) complexes isolated from three different species were electrodeposited on FTO conducting glass, forming a photoactive multilayer of the photo-electrode, for investigation of intricate electron transfer (ET) properties in such green hybrid nanosystems. The internal quantum efficiency of photo-electrochemical cells (PEC) containing the PSI-based photo-electrodes did not exceed ~ 0.5%. To reveal the reason for such a low efficiency of photocurrent generation, the temporal evolution of the transient concentration of the photo-oxidized primary electron donor, P+, was studied in aqueous suspensions of the PSI complexes by time-resolved absorption spectroscopy. The results of these measurements provided the information on: (1) completeness of charge separation in PSI reaction centers (RCs), (2) dynamics of internal charge recombination, and (3) efficiency of electron transfer from PSI to the electrolyte, which is the reaction competing with the internal charge recombination in the PSI RC. The efficiency of the full charge separation in the PSI complexes used for functionalization of the electrodes was ~ 90%, indicating that incomplete charge separation was not the main reason for the small yield of photocurrents. For the PSI particles isolated from a green alga Chlamydomonas reinhardtii, the probability of ET outside PSI was ~ 30–40%, whereas for their counterparts isolated from a cyanobacterium Synechocystis sp. PCC 6803 and a red alga Cyanidioschyzon merolae, it represented a mere ~ 4%. We conclude from the transient absorption data for the PSI biocatalysts in solution that the observed small photocurrent efficiency of ~ 0.5% for all the PECs analyzed in this study is likely due to: (1) limited efficiency of ET outside PSI, particularly in the case of PECs based on PSI from Synechocystis and C. merolae, and (2) the electrolyte-mediated electric short-circuiting in PSI particles forming the photoactive layer, particularly in the case of the C. reinhardtii PEC. Graphical abstract

Light- and Redox-Dependent Force Spectroscopy Reveals that the Interaction between Plastocyanin and Plant Photosystem I Is Favored when One Partner Is Ready for Electron Transfer

“…The redox states of PSI and Pc were respectively controlled by illuminating PSI (λ = 690 nm, power = 60 mW·cm –2 ) and using a reducing agent for Pc (sodium ascorbate, 5 mM) , (Figure B). Note that sodium ascorbate can also reduce P700 + but it does so in ∼30 s, − which is orders of magnitude longer than the typical times for Pc Ox reduction (∼3 ms), for P700 photo-oxidation (200 μs, see below), for PSI-Pc ET (10 μs), and also longer than the PSI-Pc (sample-probe) contact time in our experiments (∼25 ms). Combining these conditions, we characterized the binding event frequency and the unbinding force of the interaction between PSI and Pc in all physiological and nonphysiological redox states.…”

“…These results provide a biophysical characterization of the binding of Pc Red to PSI Ox and yield the binding event frequency and unbinding force of Pc Red to the different physiological redox forms of plant PSI. We assume that during the binding-unbinding process, the interaction analyzed under illumination is between PSI Ox and Pc Red because (i) the ET time between PSI-Pc is 10 μs, (ii) the PSI Ox -Pc Red contact time in our experimental conditions is ≈25 ms, (iii) the time for Pc Ox rereduction by ascorbate is ≈3 ms, (iv) the time for PSI reduction by ascorbate is 20–30 s − and (v) under our continuous illumination conditions, the photocurrent signal proportional to photo-oxidation saturates above 200 μs of pulsed illumination (see Supplementary Figure S2). Therefore, the probability that PSI remains oxidized during the next approach/retract cycle to acquire a force curve (which lasts 400 ms) is greater than that PSI is reduced.…”

In situ Time-Resolved Spectroelectrochemistry Reveals Limitations of Biohybrid Photoelectrode Performance

“…donor-or acceptor side of RCs-which further decrease the overall yield of photochemistry. [6][7][8] The type and extent of these bottlenecks can be assessed by examining the proportions of RCs that are open, closed, or oxidized during the operation of a device (Figure 1B). A comprehensive description of these RC states in the Rba sphaeroides RC (bRC), the limitations that induce them, and the loss processes they lead to, are described in Figure S1 and the accompanying text.…”

Spectral Dependence of the Energy Transfer from Photosynthetic Complexes to Monolayer Graphene

“…Such hybrid assemblies can be considered one of the pathways aimed at obtaining a “green” device for efficient energy conversion [ 9 ]. Indeed, a biomimetic solar cell, in which the photoactive medium is composed of photosynthetic reaction centers, could be a promising solution for conversion and storage of the sunlight energy [ 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 ]. This concept is based on the fact that photosynthetic complexes, being evolutionarily optimized for over three billion years, are highly efficient photochemical devices.…”

“…First, we designed and performed a systematic fluorescence excitation microscopy analysis, where the emission intensity was monitored for varying excitation wavelengths. Second, we carried out this analysis both for the PCP complex and for a photosystem I with its associated light-harvesting antenna (PSI–LHCI), that has been previously used in various types of biohybrid solar energy conversion devices [ 12 , 13 , 17 , 18 , 19 , 23 , 28 , 48 ]. Importantly, both pigment–protein complexes studied in this work, despite chlorophyll-based emission, differed significantly in the structure and function of the photosynthetic apparatus.…”