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

Abstract

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...

Genomic and transcriptomic insights into the survival of the subaerial cyanobacterium Nostoc flagelliforme in arid and exposed habitats

“…These cyanobacteria face extreme environments, including large temperature fluctuations and daily hydration/dehydration cycles (Murik et al, ). Desiccation‐tolerant cyanobacteria were suggested to have evolved a broad range of survival strategies to cope with these extreme conditions, including the accumulation of intracellular osmotic substances (Lebre et al, ), enhanced exopolysaccharide production and accumulation of secreted proteins in an immobilized matrix (Tamaru et al, ), and re‐modulation of energy transfer pathways by changing the states of light‐harvesting protein complexes (Bar Eyal et al, ). A better understanding of the environmental adaptations of desiccation‐tolerant cyanobacteria is relevant for developing drought‐tolerant plants and preventing desertification.…”

Macroscopic coherence as an emergent property in molecular nanotubes

“…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].…”

“…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].…”

Photosystem II core quenching in desiccated Leptolyngbya ohadii

“…In the hydrated state, the negative peak at 660 nm corresponds to APC660 and it indicates EET transfer from CPC rods to APC660. A previous study (Bar Eyal et al 2017) showed that the excitation energy is quenched within CPC rods in the desiccated state, which is reflected by the positive peak at 660 nm in Fig. 3b.…”

“…Time-resolved fluorescence of the cells was recorded at room temperature using a picosecond streak-camera system (van Stokkum et al 2008) as reported before (Bar Eyal et al 2017;Ranjbar Choubeh et al 2018), using a time window of 800 ps. The frequency-doubled output of a Ti:sapphire laser (Coherent, Mira) (800 nm) was used to excite the samples at 400 nm.…”