Electronic Energy Transfer within the Hexamer Cofactor System of Bacterial Reaction Centers

Abstract

Flow of excitation energy within the bacteriochlorin cofactor system of bacterial reaction centers has been studied by multicolor transient absorption spectroscopy using differently shaped excitation pulses of 30 fs, both at room temperature and at 15 K. This approach, which includes the analysis of free induction decay signals, helps to disentangle the processes of electronic dephasing, energy transfer, internal conversion, and nuclear motion, all taking place on the time scale of ∼100 fs. Part of the excitations (estimated at 80−90% at room temperature) flow via the scheme H* → B* → P+* → P-*, in which H* and B* represent excited bacteriopheophytin and bacteriochlorophyll monomers and P+* and P-* the upper and lower excited states of the bacteriochlorophyll dimer P, respectively. H* → B* takes less than 100 fs. B* → P+* (∼200 fs) energy transfer is a slower process than the internal conversion process within P* (50−100 fs) and therefore is rate limiting for P-* formation. At low temperature, electronic dephasing associated with the B* and P+* states takes place on a similar time scale as P* internal conversion. Upon excitation with pulses centered at 820 nm, estimated to spectrally overlap the close-lying B and P+ bands to equal extent, more than 90% of the P- band bleaches instantaneously and B* → P* transfer occurs for less than 10%. This might be indicative of an unexpectedly strong contribution of P+ to the 800 nm band. Alternatively, we propose that under these conditions the strongly coupled B* and P+* states are coherently excited. This possibility is consistent with B* → P+* electronic energy transfer occurring in the strong coupling regime under conditions where B* is more selective populated. The observed time scales are temperature-insensitive and furthermore similar in Rhodobacter sphaeroides R26 and Rhodopseudomonas viridis, which eliminates the possibility of direct B* → P-* energy transfer. At room temperature, part of the excitation energy flow deviates from the above scheme (Lin, S.; Taguchi, A. K. W; Woodbury, N. W. J. Phys. Chem. 1996, 100, 17067−17078), resulting in excitation-wavelength-dependent distributions of excited and/or radical pair states on the picosecond time scale. In general agreement with previous low-temperature work on a mutant reaction center (van Brederode, M. E.; Jones, M. R.; van Mourik, F.; van Stokkum I. H. M.; van Grondelle, R. Biochemistry 1997, 36, 6855−6861), we found that this deviation is particularly strong (up to ∼50%) at low temperature. Upon excitation in H and B, a high quantum yield is observed of radical pairs involving HL, with characteristics in the HL QY region, differing from those of P+HL- and suggesting that they can be identified as BL+HL-.