Long-Wavelength Limit of Photochemical Energy Conversion in Photosystem I

Abstract

In Photosystem I (PS I) long-wavelength chlorophylls (LWC) of the core antenna are known to extend the spectral region up to 750 nm for absorbance of light that drives photochemistry. Here we present clear evidence that even far-red light with wavelengths beyond 800 nm, clearly outside the LWC absorption bands, can still induce photochemical charge separation in PS I throughout the full temperature range from 295 to 5 K. At room temperature, the photoaccumulation of P700+• was followed by the absorbance increase at 826 nm. At low temperatures (T < 100 K), the formation of P700+•FA/B–• was monitored by the characteristic EPR signals of P700+• and FA/B–• and by the characteristic light-minus-dark absorbance difference spectrum in the QY region.P700 oxidation was observed upon selective excitation at 754, 785, and 808 nm, using monomeric and trimeric PS I core complexes of Thermosynechococcus elongatus and Arthrospira platensis, which differ in the amount of LWC. The results show that the LWC cannot be responsible for the long-wavelength excitation-induced charge separation at low temperatures, where thermal uphill energy transfer is frozen out. Direct energy conversion of the excitation energy from the LWC to the primary radical pair, e.g., via a superexchange mechanism, is excluded, because no dependence on the content of LWC was observed. Therefore, it is concluded that electron transfer through PS I is induced by direct excitation of a proposed charge transfer (CT) state in the reaction center. A direct signature of this CT state is seen in absorbance spectra of concentrated PS I samples, which reveal a weak and featureless absorbance band extending beyond 800 nm, in addition to the well-known bands of LWC (C708, C719 and C740) in the range between 700 and 750 nm. The present findings suggest that nature can exploit CT states for extending the long wavelength limit in PSI even beyond that of LWC. Similar mechanisms may work in other photosynthetic systems and in chemical systems capable of photoinduced electron transfer processes in general.

Defining the Far-red Limit of Photosystem I

“…Oxidation of P 700 was observed at 293 K and low temperatures down to 5 K by absorption and EPR spectroscopy (63). The reduction of the F A and F B iron-sulfur centers was also reported (63). The results are remarkably similar to ours.…”

“…The actual value could be even lesser due to light scattering and/or baseline correction interferences. In any case, this very low absorption alone cannot account for the quite efficient charge separation observed here and in Schlodder et al (63) in the 750 -840-nm region (20% of the P 700 ϩ formation at 820 nm at 297 K; Figs. 1 and 2).…”

“…During revision of our manuscript, we became aware of a recent study by Schlodder et al (63), who reported photochemistry in PS I to 808 nm in trimeric and monomeric core preparations from two different cyanobacterial species, Thermosynechococcus elongatus and Arthrospira platensis. Oxidation of P 700 was observed at 293 K and low temperatures down to 5 K by absorption and EPR spectroscopy (63). The reduction of the F A and F B iron-sulfur centers was also reported (63).…”

“…By using highly concentrated purified PS I core preparations, a weak and featureless absorption that extends to 850 nm was observed (63). The absorption above 750 nm was less than 0.1% of the absorption at the maximum in the Q y region at 680 nm (63).…”

“…(ii) Any role of the red Chls in the process was ruled out (at least above 800 nm). (iii) The existence of a charge transfer state responsible for the absorption and primary charge separation in this spectral region was proposed (63).…”