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Coherent phenomena in photosynthetic light harvesting: part two-observations in biological systems.

ABSTRACT: 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 "quantum 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.

SUBMITTER: Rathbone HW

PROVIDER: S-EPMC6233342 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Coherent phenomena in photosynthetic light harvesting: part two-observations in biological systems.

Rathbone Harry W HW Davis Jeffery A JA Michie Katharine A KA Goodchild Sophia C SC Robertson Neil O NO Curmi Paul M G PMG

Biophysical reviews 20180922 5

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 "quantum beats" via femtosecond laser spectroscopy, which have been o ...[more]

PMID: 30242555

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Project description:UnlabelledThe genomes of many photosynthetic and nonphotosynthetic bacteria encode numerous phytochrome superfamily photoreceptors whose functions and interactions are largely unknown. Cyanobacterial genomes encode particularly large numbers of phytochrome superfamily members called cyanobacteriochromes. These have diverse light color-sensing abilities, and their functions and interactions are just beginning to be understood. One of the best characterized of these functions is the regulation of photosynthetic light-harvesting antenna composition in the cyanobacterium Fremyella diplosiphon by the cyanobacteriochrome RcaE in response to red and green light, a process known as chromatic acclimation. We have identified a new cyanobacteriochrome named DpxA that maximally senses teal (absorption maximum, 494 nm) and yellow (absorption maximum, 568 nm) light and represses the accumulation of a key light-harvesting protein called phycoerythrin, which is also regulated by RcaE during chromatic acclimation. Like RcaE, DpxA is a two-component system kinase, although these two photoreceptors can influence phycoerythrin expression through different signaling pathways. The peak responsiveness of DpxA to teal and yellow light provides highly refined color discrimination in the green spectral region, which provides important wavelengths for photosynthetic light harvesting in cyanobacteria. These results redefine chromatic acclimation in cyanobacteria and demonstrate that cyanobacteriochromes can coordinately impart sophisticated light color sensing across the visible spectrum to regulate important photosynthetic acclimation processes.ImportanceThe large number of cyanobacteriochrome photoreceptors encoded by cyanobacterial genomes suggests that these organisms are capable of extremely complex light color sensing and responsiveness, yet little is known about their functions and interactions. Our work uncovers previously undescribed cooperation between two photoreceptors with very different light color-sensing capabilities that coregulate an important photosynthetic light-harvesting protein in response to teal, green, yellow, and red light. Other cyanobacteriochromes that have been shown to interact functionally sense wavelengths of light that are close to each other, which makes it difficult to clearly identify their physiological roles in the cell. Our finding of two photoreceptors with broad light color-sensing capabilities and clearly defined physiological roles provides new insights into complex light color sensing and its regulation.

Project description:BackgroundPhotosynthetic light-harvesting proteins are the mechanism by which energy enters the marine ecosystem. The dominant prokaryotic photoautotrophs are the cyanobacterial genera Prochlorococcus and Synechococcus that are defined by two distinct light-harvesting systems, chlorophyll-bound protein complexes or phycobilin-bound protein complexes, respectively. Here, we use the Global Ocean Sampling (GOS) Project as a unique and powerful tool to analyze the environmental diversity of photosynthetic light-harvesting genes in relation to available metadata including geographical location and physical and chemical environmental parameters.MethodsAll light-harvesting gene fragments and their metadata were obtained from the GOS database, aligned using ClustalX and classified phylogenetically. Each sequence has a name indicative of its geographic location; subsequent biogeographical analysis was performed by correlating light-harvesting gene budgets for each GOS station with surface chlorophyll concentration.Conclusion/significanceUsing the GOS data, we have mapped the biogeography of light-harvesting genes in marine cyanobacteria on ocean-basin scales and show that an environmental gradient exists in which chlorophyll concentration is correlated to diversity of light-harvesting systems. Three functionally distinct types of light-harvesting genes are defined: (1) the phycobilisome (PBS) genes of Synechococcus; (2) the pcb genes of Prochlorococcus; and (3) the iron-stress-induced (isiA) genes present in some marine Synechococcus. At low chlorophyll concentrations, where nutrients are limited, the Pcb-type light-harvesting system shows greater genetic diversity; whereas at high chlorophyll concentrations, where nutrients are abundant, the PBS-type light-harvesting system shows higher genetic diversity. We interpret this as an environmental selection of specific photosynthetic strategy. Importantly, the unique light-harvesting system isiA is found in the iron-limited, high-nutrient low-chlorophyll region of the equatorial Pacific. This observation demonstrates the ecological importance of isiA genes in enabling marine Synechococcus to acclimate to iron limitation and suggests that the presence of this gene can be a natural biomarker for iron limitation in oceanic environments.

Dataset Information

Coherent phenomena in photosynthetic light harvesting: part two-observations in biological systems.

Publications

Coherent phenomena in photosynthetic light harvesting: part two-observations in biological systems.

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