Design principles of natural light-harvesting as revealed by single molecule spectroscopy

Abstract

Biology offers a boundless source of adaptation, innovation, and inspiration. A wide range of photosynthetic organisms exist that are capable of harvesting solar light in an exceptionally efficient way, using abundant and low-cost materials. These natural light-harvesting complexes consist of proteins that strongly bind a high density of chromophores to capture solar photons and rapidly transfer the excitation energy to the photochemical reaction centre. The amount of harvested light is also delicately tuned to the level of solar radiation to maintain a constant energy throughput at the reaction centre and avoid the accumulation of the products of charge separation. In this Review, recent developments in the understanding of light harvesting by plants will be discussed, based on results obtained from single molecule spectroscopy studies. Three design principles of the main light-harvesting antenna of plants will be highlighted: (a) fine, photoactive control over the intrinsic protein disorder to efficiently use intrinsically available thermal energy dissipation mechanisms; (b) the design of the protein microenvironment of a low-energy chromophore dimer to control the amount of shade absorption; (c) the design of the exciton manifold to ensure efficient funneling of the harvested light to the terminal emitter cluster.

Quieting a noisy antenna reproduces photosynthetic light-harvesting spectra

“…27 Green sulfur bacteria thrive under precisely the same conditions for which a light harvesting antenna is finely tuned for solar power conversion. 31 overlaid on the terrestrial solar spectrum (light grey). 28…”

Local protein solvation drives direct down-conversion in phycobiliprotein PC645 via incoherent vibronic transport

“…Are there simple design principles that connect the complex atomic structure of pigment environments to the regulation of excitation energy transfer (EET) pathways in LHCs ( 1 – 5 )? As demonstrated by the environmentally assisted quantum transport (ENAQT) mechanism ( 6 ), thermally occupied low-frequency vibrations can enhance transport between energetically detuned pigments and represent the simplest design principle connecting atomistic dynamics and excitation transport.…”

Successes & challenges in the atomistic modeling of light-harvesting and its photoregulation

“…This progress has been made possible thanks to the availability of accurate structural data of the complexes, which have revealed the atomistic details not only of the protein, but also of the embedded multichromophoric aggregate responsible for absorbing and harvesting light [15]. The success of this interplay between structural data and atomistic models has been further amplified by the advent of new and more powerful spectroscopic techniques that can follow the dynamics of energy/charge transfers with a femtosecond resolution and reveal the multidimensionality of the transfer pathways with sub-nanometric resolution [16,17,18,19]. In particular, the relatively recent development of two-dimensional electronic spectroscopy (2DES) has provided a new and more incisive tool for studying energy transfer pathways in the extremely complicated LH systems, where one-dimensional techniques commonly fail in achieving a clear picture because they cannot disentangle the plethora of overlapping signals [20,21,22,23].…”