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Comparison of the Light-Harvesting Networks of Plant and Cyanobacterial Photosystem I

Melih K. ener ^*, Craig Jolley , Adam Ben-Shem , Petra Fromme , Nathan Nelson , Roberta Croce ^¶ and Klaus Schulten ^* ||

^* Beckman Institute, University of Illinois at Urbana-Champaign, Urbana, Illinois; Department of Physics and Astronomy, Arizona State University, Tempe, Arizona; Department of Biochemistry, The George S. Wise Faculty of Life Sciences, The Daniella Rich Institute for Structural Biology, Tel Aviv University, Tel Aviv, Israel; Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona; ^¶ CNR-Istituto di Biofisica, Trento, Italy; and ^|| Department of Physics, University of Illinois at Urbana-Champaign, Urbana, Illinois

Correspondence: Address reprint requests to K. Schulten, E-mail: kschulte{at}ks.uiuc.edu.

With the availability of structural models for photosystem I (PSI) in cyanobacteria and plants it is possible to compare the excitation transfer networks in this ubiquitous photosystem from two domains of life separated by over one billion years of divergent evolution, thus providing an insight into the physical constraints that shape the networks' evolution. Structure-based modeling methods are used to examine the excitation transfer kinetics of the plant PSI-LHCI supercomplex. For this purpose an effective Hamiltonian is constructed that combines an existing cyanobacterial model for structurally conserved chlorophylls with spectral information for chlorophylls in the Lhca subunits. The plant PSI excitation migration network thus characterized is compared to its cyanobacterial counterpart investigated earlier. In agreement with observations, an average excitation transfer lifetime of 49 ps is computed for the plant PSI-LHCI supercomplex with a corresponding quantum yield of 95%. The sensitivity of the results to chlorophyll site energy assignments is discussed. Lhca subunits are efficiently coupled to the PSI core via gap chlorophylls. In contrast to the chlorophylls in the vicinity of the reaction center, previously shown to optimize the quantum yield of the excitation transfer process, the orientational ordering of peripheral chlorophylls does not show such optimality. The finding suggests that after close packing of chlorophylls was achieved, constraints other than efficiency of the overall excitation transfer process precluded further evolution of pigment ordering.

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