The CP43 Proximal Antenna Complex of Higher Plant Photosystem II Revisited: Modeling and Hole Burning Study. I

Abstract

The CP43 core antenna complex of Photosystem II is known to possess two quasi-degenerate "red"-trap states [R. Jankowiak et al. J. Phys. Chem. B 2000, 104, 11805]. It has been suggested recently [V. Zazubovich and R. Jankowiak, J. Lum. 2007, 127, 245] that the site distribution functions (SDFs) of the red states (A and B) are uncorrelated and that narrow holes are burned in the subpopulations of chlorophylls (Chls) from states A and B that are the lowestenergy Chl in their complex and previously thought not to transfer energy. This model of uncorrelated excitation energy transfer (EET) between the quasi-degenerate bands is expanded by taking into account both electron-phonon and vibrational coupling. The model is applied to fit simultaneously absorption, emission, zero-phonon action, and transient hole burned (HB) spectra obtained for the CP43 complex with minimized contribution from aggregation. It is demonstrated that the above listed spectra can be well fitted using the uncorrelated EET model, providing strong evidence for the existence of efficient energy transfer between the two lowest energy states A and B (either from A to B or from B to A) in CP43. Possible candidate Chls for the low-energy A and B states are discussed, providing a link between CP43 structure and spectroscopy. Finally, we propose that persistent holes originate from regular NPHB accompanied by the redistribution of oscillator strength due to excitonic interactions, rather than photoconversion involving Chl-protein hydrogen bonding as suggested before [J.L. Hughes et al., Biochemistry 45, 12345, 2006]. In the accompanying paper (II) it is demonstrated that the model discussed in this manuscript is consistent with excitonic calculations, which also provide very good fits to both transient and persistent HB spectra obtained under non-line narrowing conditions.

Structure-based simulation of linear optical spectra of the CP43 core antenna of photosystem II

“…This assignment is in agreement with spectroscopic properties of low-energy excited states in CP43 (Groot et al 1999;Jankowiak et al 2000;Hughes et al 2006;Dang et al 2008) and earlier fits of linear and non-linear spectra (Raszewski and Renger 2008), but remains tentative due to our limited knowledge of structural details. The analysis of electrostatic pigmentprotein interactions in CP43 suggests target sites for future mutagenesis experiments that may help to sharpen the assignment of site energies and deepen our understanding of the PSIIcc core antenna.…”

“…Parameters: r = 120 cm -1 , V c = 20 cm -1 , S = 0.5 more than one red-shifted Chl. This finding is in agreement with spectral hole-burning experiments, which were interpreted in terms of two quasidegenerate and weakly coupled trap states designated A and B (Jankowiak et al 2000), as well as with earlier spectral deconvolutions (Groot et al 1999) and more recent hole-burning studies (Hughes et al 2006;Dang et al 2008). Raszewski and Renger identified the A state with an exciton state dominated by the lowenergy Chl 37 and the B state with that of Chls 43 and 45 based on differences in hole-burning and triplet formation efficiencies.…”

“…Groot et al (1999) investigated CP43 with fluorescence line narrowing spectroscopy. They observed a variation of the line-narrowing pattern with excitation wavelength, which they ascribed to the presence of two different pools of emitting Chls in agreement with their deconvolution of the absorption spectrum and the more recent hole-burning data (Jankowiak et al 2000;Hughes et al 2006;Dang et al 2008). They also found evidence that at least one of the emitting Chls has its 13 1 -keto group involved in a hydrogen bond with the protein environment.…”

“…Indeed, Dang et al (2008) observed a dependence of the peak intensity at 683 nm and spectral width in this region on the preparation history of their CP43 samples. Also, there is a consensus that the two emitting states A and B have a significantly different inhomogeneous width (Jankowiak et al 2000;Hughes et al 2006;Dang et al 2008). The conformational flexibility of DGDG could cause a large inhomogeneous broadening of a nearby Chl.…”

“…A key problem of current research on this system is to understand, how the protein matrix modulates the properties of the chlorophyll (Chl) a molecules bound to CP43 and CP47 to allow for efficient excitation energy transfer (EET) (Raszewski and Renger 2008;Renger and Renger 2008). The advantage of PSIIcc is that it can be decomposed, enabling the study of the photophysical properties of the separated core antennae (Alfonso et al 1994;Groot et al 1999;Dang et al 2008;Reppert et al 2008;Casazza et al 2010;Jankowiak et al 2000;Hughes et al 2006).…”