Direct Evidence for Excitation Energy Transfer Limitations Imposed by Low-Energy Chlorophylls in Photosystem I-Light Harvesting Complex I of Land Plants.

Mattia Russo,Anna Paola Casazza,Margherita Maiuri,Stefano Santabarbara,Giulio Cerullo

doi:10.1021/acs.jpcb.1c01498

Abstract

The overall efficiency of photosynthetic energy conversion depends both on photochemical and excitation energy transfer processes from extended light-harvesting antenna networks. Understanding the trade-offs between increase in the antenna cross section and bandwidth and photochemical conversion efficiency is of central importance both from a biological perspective and for the design of biomimetic artificial photosynthetic complexes. Here, we employ two-dimensional electronic spectroscopy to spectrally resolve the excitation energy transfer dynamics and directly correlate them with the initial site of excitation in photosystem I–light harvesting complex I (PSI-LHCI) supercomplex of land plants, which has both a large antenna dimension and a wide optical bandwidth extending to energies lower than the peak of the reaction center chlorophylls. Upon preferential excitation of the low-energy chlorophylls (red forms), the average relaxation time in the bulk supercomplex increases by a factor of 2–3 with respect to unselective excitation at higher photon energies. This slowdown is interpreted in terms of an excitation energy transfer limitation from low-energy chlorophyll forms in the PSI-LHCI. These results aid in defining the optimum balance between the extension of the antenna bandwidth to the near-infrared region, which increases light-harvesting capacity, and high photoconversion quantum efficiency.

Highlights

Photosystem I (PSI) is one of the two pigment−protein supercomplexes essential for oxygenic photosynthesis, which mediate the light-driven electron transport from water to NADP+
PSI is an intriguing system from the photochemical perspective, because it operates with an extremely high photon conversion quantum efficiency, approaching unity, even in the presence of energy states in its antenna network that absorb at lower energy than the chromophore involved in photochemical conversion
Thermodynamic reasoning would imply a competition for localization of the excited states between the reaction center (RC) and the low-energy Chl red forms, which should decrease the photon conversion quantum efficiency

Summary

Introduction

Photosystem I (PSI) is one of the two pigment−protein supercomplexes essential for oxygenic photosynthesis, which mediate the light-driven electron transport from water to NADP+. The PSI-LHCI supercomplex is considered as one of the best performing photochemical machineries known in nature, showing the highest efficiency among other photosystems, approaching unity.[1−3] This very high photon conversion yield is maintained even though some light-harvesting antenna pigments absorb at lower energies than the RC chlorophylls (Chl), implying a thermodynamically unfavorable uphill excitation energy transfer (EET) to the photocatalytic site.[4] In higher plants, these low-energy absorbing chromophores, often referred to as “red forms”, are mainly located in the LHCI antenna,[4−6] and are from a structural perspective, located at the periphery of the complex.[7] more than one lowenergy state is present in the LHCI, and each of the two dimers (Lhca1/Lhca[4] and Lhca2/Lhca3) comprising it appears to bind a long-wavelength spectral form emitting at ∼730/735 nm.[8] This scenario is different from the case of cyanobacterial PSI, where the red forms, whose exact characteristics are species-dependent,[9] are instead located in the core complex, and spatially closer to the RC

Methods

Results

Conclusion