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...

Cyanobacteria use chlorophyll and phycobiliproteins to harvest light. The resulting excitation energy is delivered to reaction centers (RCs), where photochemistry starts. The relative amounts of excitation energy arriving at the RCs of photosystem I (PSI) and II (PSII) depend on the spectral composition of the light. To balance the excitations in both photosystems, cyanobacteria perform state transitions to equilibrate the excitation energy. They go to state I if PSI is preferentially excited, for example after illumination with blue light (light I), and to state II after illumination with green-orange light (light II) or after dark adaptation. In this study, we performed 77-K time-resolved fluorescence spectroscopy on wild-type Synechococcus elongatus 7942 cells to measure how state transitions affect excitation energy transfer to PSI and PSII in different light conditions and to test the various models that have been proposed in literature. The time-resolved spectra show that the PSII core is quenched in state II and that this is not due to a change in excitation energy transfer from PSII to PSI (spill-over), either direct or indirect via phycobilisomes.

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Cyanobacteria living in the harsh environment of the desert have to protect themselves against high light intensity and prevent photodamage. These cyanobacteria are in a desiccated state during the largest part of the day when both temperature and light intensity are high. In the desiccated state, their photosynthetic activity is stopped, whereas upon rehydration the ability to perform photosynthesis is regained. Earlier reports indicate that light-induced excitations in Leptolyngbya ohadii are heavily quenched in the desiccated state, because of a loss of structural order of the light-harvesting phycobilisome structures (Bar Eyal et al. in Proc Natl Acad Sci 114:9481, 2017) and via the stably oxidized primary electron donor in photosystem I, namely P700 + (Bar Eyal et al. in Biochim Biophys Acta Bioenergy 1847:1267-1273, 2015). In this study, we use picosecond fluorescence experiments to demonstrate that a third protection mechanism exists, in which the core of photosystem II is quenched independently.