Robustness and Optimality of Light Harvesting in Cyanobacterial Photosystem I

Abstract

As most biological species, photosynthetic lifeforms have evolved to function optimally, despite thermal disorder and with fault tolerance. It remains a challenge to understand how this is achieved. To address this challenge the function of the protein-pigment complex photosystem I (PSI) of the cyanobacterium Synechococcus elongatus is investigated theoretically. The recently obtained high resolution structure of this complex exhibits an aggregate of 96 chlorophylls that are electronically coupled to function as a light-harvesting antenna complex. This paper constructs an effective Hamiltonian for the chlorophyll aggregate to describe excitation transfer dynamics and spectral properties of PSI. For this purpose, a new kinetic expansion method, the sojourn expansion, is introduced. Our study shows that at room temperature fluctuations of site energies have little effect on the calculated excitation lifetime and quantum yield, which compare favorably with experimental results. The efficiency of the system is found to be robust against 'pruning' of individual chlorophylls. An optimality of the arrangement of chlorophylls is identified through the quantum yield in comparison with an ensemble of randomly oriented chlorophylls, though, the quantum yield is seen to change only within a narrow interval in such an ensemble.

Lateral Segregation of Photosystem I in Cyanobacterial Thylakoids

“…where N Chl ¼ 96 is the number of chlorophylls in one monomer (Sener et al, 2004;Damjanović et al, 2002;Sener et al, 2002) . Figure 4A illustrates the couplings V MN;mn across the five monomers, I, II, III, II', and III', as labeled in Figure 4B.…”

“…The cross-monomer trapping probabilities p M;m;N describe the level of excitation sharing between neighboring monomers and are plotted in Figure 4C for the reference monomer N ¼ I. The cross-trapping probabilities averaged over each monomer Figure 3) does not provide a significant improvement of quantum yield (Supplemental Figure 7E) over that of an isolated trimer (Sener et al, 2002) due to the short trapping time of PSI. Since the quantum yields for the observed trimer array ( Figure 3) and for isolated trimers are nearly identical, the primary role of the trimer packing pattern appears to maximize the packing efficiency of PSI complexes in the membrane rather than to facilitate intertrimer energy transfer.…”

“…The intermonomer couplings, V MN;mn ; MÞN; were computed using the transitiondipole approximation according to Sener et al (2004). Excitation transfer kinetics in the PSI arrays can be described using Förster theory as an approximation (Sener et al, 2002(Sener et al, , 2004Croce and van Amerongen, 2013;Yang et al, 2003;van Stokkum et al, 2013). where J MN;mn are the spectral overlap integrals defined by Sener et al (2004).…”

Robustness, efficiency, and optimality in the Fenna-Matthews-Olson photosynthetic pigment-protein complex

“…6,20,21,27,28 The effect of removing a chromophore on EET efficiency has also been investigated, and it has been suggested that photosynthetic EET networks display a robustness to the loss of a chromophore in the network through the utilisation of multiple EET pathways. 6,[29][30][31][32] In contrast to these previous investigations, which have focussed on the role of site energy fluctuations, environmental fluctuations, and exciton trapping rates, this article focusses predominantly on evaluating how the electronic Hamiltonian of the EET system governs the robustness and optimal EET characteristics of a biological photosynthetic system. Specifically, we adopt a network-based view of photosynthetic EET systems and focus on investigating quantum transport dynamics in a prototypical PPC, the FMO complex.…”

Reaction paths based on mean first-passage times

“…We build the transition matrix K xy by using the inter-chlorophyll excitation transfer rates that were calculated in Ref. [22] based on the theory developed in [23] and the recently obtained structure of photosystem I [24]. The MFPT τ x from chlorophyll x to the P700 pair is then [20] …”