An easily reversible structural change underlies mechanisms enabling desert crust cyanobacteria to survive desiccation

Bar-Eyal, Leeat; Eisenberg, Ido; Faust, Adam; Raanan, Hagai; Nevo, Reinat; Rappaport, Fabrice; Krieger‐Liszkay, Anja; Sétif, Pièrre; Thurotte, Adrien; Reich, Ziv; Kaplan, Aaron; Ohad, Itzhak; Paltiel, Yossi; Keren, Nir

doi:10.1016/j.bbabio.2015.07.008

Cited by 46 publications

(47 citation statements)

References 42 publications

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“…However, this is not the only protective mechanism at play in the desiccated state. Our data also indicated a strong quenching reaction in the phycobilisome (PBS) lightharvesting antenna (7).…”

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confidence: 59%

“…A study of this process indicated similar absorption cross-sections for desiccated and hydrated cyanobacteria; that is, L. ohadii absorbs a similar amount of light energy per wavelength when hydrated and when desiccated (7). Nevertheless, in the desiccated state electron transport is shut down, and fluorescence yield decreases by ∼70%.…”

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confidence: 97%

“…However, as temperatures elevate, water quickly evaporates. Such conditions can be extremely harmful for photosynthetic organisms and require adaptations on all cellular levels (3)(4)(5)(6)(7)(8)(9). These include shifts in metabolic profiles and the accumulation of compatible solutes.…”

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confidence: 99%

“…To maintain L. ohadii cells in a viable state the desiccation process must be gradual (3). Recovery of photosynthetic activity, on the other hand, can occur immediately upon the addition of water (7). The desiccation/hydration transition does not require the breakdown and renewed production of photosynthetic protein complexes or pigments and allows L. ohadii to use the short time of morning hydration for photosynthesis and avoid photodamage during the remainder of the day (4).…”

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confidence: 99%

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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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confidence: 59%

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confidence: 97%

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confidence: 99%

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confidence: 99%

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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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“…This cessation of photosynthetic electron transport is thought to be a requisite response to prevent the photodamage of the photosynthetic machinery (Fukuda et al, 2008;Hirai et al, 2004). However, the mechanism that regulates photosynthesis in response to desiccation still needs to be elucidated (Bar-Eyal et al, 2015;Raanan et al, 2016).…”

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confidence: 99%

Characterization of extracellular matrix components from the desiccation-tolerant cyanobacterium <i>Nostoc commune</i>

Inoue-Sakamoto

Tanji

Yamaba

et al. 2018

J. Gen. Appl. Microbiol.

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The terrestrial cyanobacterium Nostoc commune forms macroscopic colonies in its natural habitats, and these colonies consist of both cellular filaments and massive extracellular matrixes. In this study, the biochemical features of the extracellular matrix components were investigated. Naturally growing N. commune was tolerant to desiccation, and produced massive extracellular polysaccharides that contained both neutral sugars and glucuronic acid as constituent monosaccharides. The extracellular polysaccharide contents and desiccation tolerance were compared in laboratory culture strains of Nostoc species. The laboratory culture of N. commune strain KU002 was sensitive to desiccation and produced smaller amounts of extracellular polysaccharides, unlike the field-isolated naturally growing colonies. Nostoc punctiforme strain M-15, which is genetically closed to N. commune, was able to tolerate desiccation, although the other Nostoc strains were desiccation-sensitive. A laboratory culture strain of the aquatic cyanobacterium Nostoc sphaericum produced massive extracellular polysaccharides but was sensitive to desiccation, suggesting that extracellular matrix production is not enough to make this strain tolerant to desiccation. WspA (water stress protein) and SodF (superoxide dismutase) were found to be characteristic protein components of the extracellular matrix of N. commune. Because the WspA proteins were heterogeneous, the wspA genes were highly diverse among the different genotypes of N. commune, although the sodF gene was rather conservative. The heterogeneity of the WspA proteins suggests their complex roles in the environmental adaptation mechanism in N. commune.

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Co‐cultivation of diazotrophic terrestrial cyanobacteria and Arabidopsis thaliana

Strieth

Nonno

Stiefelmaier

et al. 2020

Engineering in Life Sciences

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Diazotrophic cyanobacteria are able to fix N2 from the atmosphere and release it as bioavailable nitrogen what other organisms can utilize. Thus, they could be used as living nitrogen supplier whereby the use of fertilizer could be reduced in agricultural industry what results in a decrease of laughing gas released during fertilizer production. The diazotroph cyanobacterium Desmonostoc muscorum (D. muscorum) was characterized in shake flasks cultivated in nitrogen‐free and nitrogen‐containing medium. Similar growth rates were reached in both cultivations and the release of ammonium by D. muscorum was detected under nitrogen depletion. Subsequently, D. muscorum was co‐cultivated with Arabidopsis thaliana (A. thaliana) in nitrogen‐free medium. Additionally, the plant was cultivated in nitrogen containing and nitrogen‐free medium without D. muscorum as reference. A co‐cultivation led to higher growth rates of the cyanobacterium and similar growth of A. thaliana with similar maximum photochemical efficiency of photosystem II compared to the growth of nitrogen containing medium. Further, accumulation of cyanobacterial cells around the roots of A. thaliana was detected, indicating a successfully induced artificial symbiosis. Based on these results, D. muscorum could be a promising cyanobacterium as living nitrogen supplier for plants.

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An easily reversible structural change underlies mechanisms enabling desert crust cyanobacteria to survive desiccation

Cited by 46 publications

References 42 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

Characterization of extracellular matrix components from the desiccation-tolerant cyanobacterium <i>Nostoc commune</i>

Co‐cultivation of diazotrophic terrestrial cyanobacteria and Arabidopsis thaliana

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