Considerable debate surrounds the question of whether or not quantum mechanics plays a significant, non-trivial role in photosynthetic light harvesting. Many have proposed that quantum superpositions and/or quantum transport phenomena may be responsible for the efficiency and robustness of energy transport present in biological systems. The critical experimental observations comprise the observation of coherent oscillations or Bquantum beats^via femtosecond laser spectroscopy, which have been observed in many different light harvesting systems. Part Two of this review aims to provide an overview of experimental observations of energy transfer in the most studied light harvesting systems. Length scales, derived from crystallographic studies, are combined with energy and time scales of the beats observed via spectroscopy. A consensus is emerging that most long-lived (hundreds of femtoseconds) coherent phenomena are of vibrational or vibronic origin, where the latter may result in coherent excitation transport within a protein complex. In contrast, energy transport between proteins is likely to be incoherent in nature. The question of whether evolution has selected for these non-trivial quantum phenomena may be an unanswerable question, as dense packings of chromophores will lead to strong coupling and hence non-trivial quantum phenomena. As such, one cannot discern whether evolution has optimised light harvesting systems for high chromophore density or for the ensuing quantum effects as these are inextricably linked and cannot be switched off.
In addition to their membrane‐bound chlorophyll a/c light‐harvesting antenna, the cryptophyte algae have evolved a unique phycobiliprotein antenna system located in the thylakoid lumen. The basic unit of this antenna consists of two copies of an αβ protomer where the α and β subunits scaffold different combinations of a limited number of linear tetrapyrrole chromophores. While the β subunit is highly conserved, encoded by a single plastid gene, the nuclear‐encoded α subunits have evolved diversified multigene families. It is still unclear how this sequence diversity results in the spectral diversity of the mature proteins. By careful examination of three newly determined crystal structures in comparison with three previously obtained, we show how the α subunit amino acid sequences control chromophore conformations and hence spectral properties even when the chromophores are identical. Previously we have shown that α subunits control the quaternary structure of the mature αβ.αβ complex (either open or closed), however, each species appeared to only harbor a single quaternary form. Here we show that species of the Hemiselmis genus contain expressed α subunit genes that encode both distinct quaternary structures. Finally, we have discovered a common single‐copy gene (expressed into protein) consisting of tandem copies of a small α subunit that could potentially scaffold pairs of light harvesting units. Together, our results show how the diversity of the multigene α subunit family produces a range of mature cryptophyte antenna proteins with differing spectral properties, and the potential for minor forms that could contribute to acclimation to varying light regimes.
Photosynthetic organisms have developed diverse antennas composed of chromophorylated proteins to increase photon capture. Cryptophyte algae acquired their photosynthetic organelles (plastids) from a red alga by secondary endosymbiosis. Cryptophytes lost the primary red algal antenna, the red algal phycobilisome, replacing it with a unique antenna composed of αβ protomers, where the β subunit originates from the red algal phycobilisome. The origin of the cryptophyte antenna, particularly the unique α subunit, is unknown. Here we show that the cryptophyte antenna evolved from a complex between a red algal scaffolding protein and phycoerythrin β. Published cryo-EM maps for two red algal phycobilisomes contain clusters of unmodelled density homologous to the cryptophyte-αβ protomer. We modelled these densities, identifying a new family of scaffolding proteins related to red algal phycobilisome linker proteins that possess multiple copies of a cryptophyte-α-like domain. These domains bind to, and stabilise, a conserved hydrophobic surface on phycoerythrin β, which is the same binding site for its primary partner in the red algal phycobilisome, phycoerythrin α. We propose that after endosymbiosis these scaffolding proteins outcompeted the primary binding partner of phycoerythrin β, resulting in the demise of the red algal phycobilisome and emergence of the cryptophyte antenna.
The role of non-trivial quantum mechanical effects in biology has been the subject of intense scrutiny over the past decade. Much of the focus on potential "quantum biology" has been on energy transfer processes in photosynthetic light harvesting systems. Ultrafast laser spectroscopy of several light harvesting proteins has uncovered coherent oscillations dubbed "quantum beats" that persist for hundreds of femtoseconds and are putative signatures for quantum transport phenomena. This review describes the language and basic quantum mechanical phenomena that underpin quantum transport in open systems such as light harvesting and photosynthetic proteins, including the photosystem reaction centre. Coherent effects are discussed in detail, separating various meanings of the term, from delocalized excitations, or excitons, to entangled states and coherent transport. In particular, we focus on the time, energy and length scales of energy transport processes, as these are critical in understanding whether or not coherent processes are important. The role played by the protein in maintaining chromophore systems is analysed. Finally, the spectroscopic techniques that are used to probe energy transfer dynamics and that have uncovered the quantum beats are described with reference to coherent phenomena in light harvesting.
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