Light Absorption and Energy Transfer in the Antenna Complexes of Photosynthetic Organisms

Abstract

The process of photosynthesis is initiated by the capture of sunlight by a network of light-absorbing molecules (chromophores), which are also responsible for the subsequent funneling of the excitation energy to the reaction centers. Through evolution, genetic drift, and speciation, photosynthetic organisms have discovered many solutions for light harvesting. In this review, we describe the underlying photophysical principles by which this energy is absorbed, as well as the mechanisms of electronic excitation energy transfer (EET). First, optical properties of the individual pigment chromophores present in light-harvesting antenna complexes are introduced, and then we examine the collective behavior of pigment-pigment and pigment-protein interactions. The description of energy transfer, in particular multichromophoric antenna structures, is shown to vary depending on the spatial and energetic landscape, which dictates the relative coupling strength between constituent pigment molecules. In the latter half of the article, we focus on the light-harvesting complexes of purple bacteria as a model to illustrate the present understanding of the synergetic effects leading to EET optimization of light-harvesting antenna systems while exploring the structure and function of the integral chromophores. We end this review with a brief overview of the energy-transfer dynamics and pathways in the light-harvesting antennas of various photosynthetic organisms.

Using coherence to enhance function in chemical and biophysical systems

“…The delocalization of excitation within donor and/or acceptor manifolds enables remarkable acceleration of the energy transfer rate because the collective transition dipoles are much larger than molecular transition dipoles. Also, in marked contrast to Förster theory, dark exciton states are often similarly good excitation donors or acceptors because of how the dipole approximation fails to account for the structure of molecular aggregates 64 . For B800 to B850 energy transfer in LH2, the rate is predicted to be ten times faster than the simulations that assume excitation is localized on bacteriochlorophyll molecules 65 .…”

“…Instead, the energy donor and/or acceptor comprise the exciton states shared between strongly interacting chromophores. New effective chromophores for light harvesting can thus be constructed, or in nature they can evolve based on pigments already employed by a photosynthetic organism-amply demonstrated by the B850 ring in the LH2 light-harvesting complex of purple bacteria 64 . A modified version of Förster theory accounts for the way these non-additive effects in excitonic donors and acceptors promote energy transfer, and we call this the Generalized Förster Theory (GFT) [64][65][66] .…”

“…New effective chromophores for light harvesting can thus be constructed, or in nature they can evolve based on pigments already employed by a photosynthetic organism-amply demonstrated by the B850 ring in the LH2 light-harvesting complex of purple bacteria 64 . A modified version of Förster theory accounts for the way these non-additive effects in excitonic donors and acceptors promote energy transfer, and we call this the Generalized Förster Theory (GFT) [64][65][66] . In GFT, the donor and/or acceptor states are delocalized-this is strong electronic coherence-but owing to a separation of timescales (energy scales of electronic couplings) the energy transfer from donor to acceptor is treated as incoherent, just as in Förster theory.…”

Contribution of low-temperature single-molecule techniques to structural issues of pigment–protein complexes from photosynthetic purple bacteria

“…The photosynthetic apparatus of purple bacteria has inspired many researchers, because it represents a relatively simple model system to study the key features of energy-and charge transfer processes in photosynthesis [1][2][3][4][5][6]. For most of these bacteria one distinguishes a peripheral complex (LH2) and a core complex (RC-LH1) that are associated with the primary photosynthetic processes.…”

Introduction: light harvesting for photosynthesis

“…Plants and photosynthetic algae also developed strategies to acclimate to varying light conditions during seasons and can rapidly adjust their antenna sizes in case of excess light, avoiding over-excitation and formation of harmful byproducts. To date, the combination of spectroscopic data with high-resolution structures of various antenna complexes has strongly improved our understanding of the process of excitation energy transfer and inspired design of solar materials (Mirkovic et al 2017). However, the adaptive and regulatory mechanisms by which light-harvesting antenna systems respond to variations in light intensity and quality, redirect excitation-transfer pathways and dissipate excess excitation energy still have many unsolved questions.…”