Regulating the Energy Flow in a Cyanobacterial Light-Harvesting Antenna Complex

Eisenberg, Ido; Caycedo‐Soler, Felipe; Harris, Daniel K.; Yochelis, Shira; Huelga, Susana F.; Plenio, Martin B.; Adir, Noam; Keren, Nir; Paltiel, Yossi

doi:10.1021/acs.jpcb.6b10590

Cited by 29 publications

(30 citation statements)

References 49 publications

(95 reference statements)

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“…PC is known to be sensitive to the ionic or dielectric properties of its environment (34). However, changes in these properties during desiccation are not expected to lead to the dramatic fluorescence quenching observed here (Fig.…”

Section: Discussionmentioning

confidence: 64%

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Changes in aggregation states of light-harvesting complexes as a mechanism for modulating energy transfer in desert crust cyanobacteria

Eyal

Choubeh

Cohen

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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In this paper we propose an energy dissipation mechanism that is completely reliant on changes in the aggregation state of the phycobilisome light-harvesting antenna components. All photosynthetic organisms regulate the efficiency of excitation energy transfer (EET) to fit light energy supply to biochemical demands. Not many do this to the extent required of desert crust cyanobacteria. Following predawn dew deposition, they harvest light energy with maximum efficiency until desiccating in the early morning hours. In the desiccated state, absorbed energy is completely quenched. Time and spectrally resolved fluorescence emission measurements of the desiccated desert crust Leptolyngbya ohadii strain identified (i) reduced EET between phycobilisome components, (ii) shorter fluorescence lifetimes, and (iii) red shift in the emission spectra, compared with the hydrated state. These changes coincide with a loss of the ordered phycobilisome structure, evident from small-angle neutron and X-ray scattering and cryo-transmission electron microscopy data. Based on these observations we propose a model where in the hydrated state the organized rod structure of the phycobilisome supports directional EET to reaction centers with minimal losses due to thermal dissipation. In the desiccated state this structure is lost, giving way to more random aggregates. The resulting EET path will exhibit increased coupling to the environment and enhanced quenching.eserts cover almost half of the Earth's terrestrial surface, and although desert conditions may seem unfavorable, they are home for diverse ecosystems. Many of these ecosystems are founded on biological desert crusts, which play an essential role in stabilizing shifting sands and enriching them with nutrients (1, 2). Cyanobacteria are among the first microorganisms to inhabit these crusts where one of the major sources of water is often dew deposited before dawn (3, 4). However, as temperatures elevate, water quickly evaporates. Such conditions can be extremely harmful for photosynthetic organisms and require adaptations on all cellular levels (3-9). These include shifts in metabolic profiles and the accumulation of compatible solutes. A key issue is the adaptation of the photosynthetic apparatus because continued photosynthetic activity under high light, and especially in combination with desiccation, may lead to the production of reactive oxygen species that will cause damage to the entire cell (10-12). The cyanobacteria that colonize sand crusts evolved strategies for coping with these daily cycles of hydration using mechanisms that enable extensive quenching of absorbed light energy. The extent of quenching in these organisms far exceeds that of common laboratory model organisms (13, 14).Our studies focused on Leptolyngbya ohadii, a crust cyanobacterium isolated from the Nizzana region of the NW Negev desert in Israel (3,6). This is a keystone organism in this environment (4). To maintain L. ohadii cells in a viable state the desiccation process must be gradual (3). Recovery o...

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Section: Discussionmentioning

confidence: 64%

“…We can draw corollaries from in vitro studies in which we controlled the aggregation state of PC and APC artificially (34). Aggregation of PC in solution leads to shortening of their lifetime, red shift, and a lower fluorescence yield.…”

Section: Discussionmentioning

confidence: 99%

Changes in aggregation states of light-harvesting complexes as a mechanism for modulating energy transfer in desert crust cyanobacteria

Eyal

Choubeh

Cohen

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Quenching and radiative decay are taken from the experimental fitting of Ref. [47] as a biexponential decay, with time constants of 0.8ns and 1.7ns, and a relative weight of 60% and 40%, respectively. As mentioned above, the spectral properties of the bilin pigments highly depend on their environment, i.e.…”

Section: Excitation Transfer In Phycobilisome Rodsmentioning

confidence: 99%

Light Adaptation in Phycobilisome Antennas: Influence on the Rod Length and Structural Arrangement

et al. 2017

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Phycobilisomes, the light-harvesting antennas of cyanobacteria, can adapt to a wide range of environments thanks to a composition and function response to stress conditions. We study how structural changes influence excitation transfer in these super-complexes. Specifically, we show the influence of the rod length on the photon absorption and subsequent excitation transport to the core. Despite the fact that the efficiency of individual disks on the rod decreases with increasing rod length, we find an optimal length for which the average rod efficiency is maximal. Combining this study with experimental structural measurements, we propose models for the arrangement of the phycobiliproteins inside the thylakoid membranes, evaluate the importance of rod length, and predict the corresponding transport properties for different cyanobacterial species. This analysis, which links the functional and structural properties of full phycobilisome complexes, thus provides further rationals to help resolving their exact structure.

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“…Molecular nanotubes are among the most interesting and most investigated structures. They are present in several natural photosynthetic complexes, for instance in the Green Sulphur Bacteria [4][5][6][7][8][9][10][11] or in Phycobilisome Antennas [12][13][14][15]. They are also present in other biomolecular systems, for instance in Microtubules, which are fundamental biological structures, showing interesting similarities with photosynthetic Antenna complexes [16,17].…”

Section: Introductionmentioning

confidence: 99%

“…Green Sulphur bacteria are photosynthetic organisms which live in deep water where the sunlight flux is very low [5] and they are among the most efficient photosynthetic systems [6][7][8]. Similarly to other antenna complexes present in nature [12][13][14][15], they present a high degree of symmetry being arranged in nontrivial cylindrical structures with an ordered orientation of the molecule dipoles. We analyse both the wild type (WT) and the triple mutant type (MT), which have been recently investigated in [53,54].…”

Section: Introductionmentioning

confidence: 99%

Macroscopic coherence as an emergent property in molecular nanotubes

et al. 2019

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Nanotubular molecular self-aggregates are characterized by a high degree of symmetry and they are fundamental systems for light-harvesting and energy transport. While coherent effects are thought to be at the basis of their high efficiency, the relationship between structure, coherence and functionality is still an open problem. We analyse natural nanotubes present in Green Sulphur Bacteria. We show that they have the ability to support macroscopic coherent states, i.e. delocalized excitonic states coherently spread over many molecules, even at room temperature. Specifically, assuming a canonical thermal state we find, in natural structures, a large thermal coherence length, of the order of 1000 molecules. By comparing natural structures with other mathematical models, we show that this macroscopic coherence cannot be explained either by the magnitude of the nearest-neighbour coupling between the molecules, which would induce a thermal coherence length of the order of 10 molecules, nor by the presence of long-range interactions between the molecules. Indeed we prove that the existence of macroscopic coherent states is an emergent property of such structures due to the interplay between geometry and cooperativity (superradiance and super-transfer). In order to prove that, we give evidence that the lowest part of the spectrum of natural systems is determined by a cooperatively enhanced coupling (super-transfer) between the eigenstates of modular sub-units of the whole structure. Due to this enhanced coupling strength, the density of states is lowered close to the ground state, thus boosting the thermal coherence length. As a striking consequence of the lower density of states, an energy gap between the excitonic ground state and the first excited state emerges. Such energy gap increases with the length of the nanotube (instead of decreasing as one would expect), up to a critical system size which is close to the length of the natural complexes considered.

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Regulating the Energy Flow in a Cyanobacterial Light-Harvesting Antenna Complex

Cited by 29 publications

References 49 publications

Changes in aggregation states of light-harvesting complexes as a mechanism for modulating energy transfer in desert crust cyanobacteria

Changes in aggregation states of light-harvesting complexes as a mechanism for modulating energy transfer in desert crust cyanobacteria

Light Adaptation in Phycobilisome Antennas: Influence on the Rod Length and Structural Arrangement

Macroscopic coherence as an emergent property in molecular nanotubes

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