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Influence of Chemically Disrupted Photosynthesis on Cyanobacterial Thylakoid Dynamics in Synechocystis sp. PCC 6803.

ABSTRACT: The photosynthetic machinery of the cyanobacterium Synechocystis sp. PCC 6803 resides in flattened membrane sheets called thylakoids, situated in the peripheral part of the cellular cytoplasm. Under photosynthetic conditions these thylakoid membranes undergo various dynamical processes that could be coupled to their energetic functions. Using Neutron Spin Echo Spectroscopy (NSE), we have investigated the undulation dynamics of Synechocystis sp. PCC 6803 thylakoids under normal photosynthetic conditions and under chemical treatment with DCMU (3-(3,4-dichlorophenyl)-1,1-dimethylurea), an herbicide that disrupts photosynthetic electron transfer. Our measurements show that DCMU treatment has a similar effect as dark conditions, with differences in the undulation modes of the untreated cells compared to the chemically inhibited cells. We found that the disrupted membranes are 1.5-fold more rigid than the native membranes during the dark cycle, while in light they relax approximately 1.7-fold faster than native and they are 1.87-fold more flexible. The strength of the herbicide disruption effect is characterized further by the damping frequency of the relaxation mode and the decay rate of the local shape fluctuations. In the dark, local thicknesses and shape fluctuations relax twice as fast in native membranes, at 17% smaller mode amplitude, while in light the decay rate of local fluctuations is 1.2-fold faster in inhibited membranes than in native membranes, at 56% higher amplitude. The disrupted electron transfer chain and the decreased proton motive force within the lumenal space partially explain the variations observed in the mechanical properties of the Synechocystis membranes, and further support the hypothesis that the photosynthetic process is tied to thylakoid rigidity in this type of cyanobacterial cell.

SUBMITTER: Stingaciu LR

PROVIDER: S-EPMC6450941 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:In recent years, there has been an increased interest in the research and development of sustainable alternatives to fossil fuels. Using photosynthetic microorganisms to produce such alternatives is advantageous, since they can achieve direct conversion of carbon dioxide from the atmosphere into the desired product, using sunlight as the energy source. Squalene is a naturally occurring 30-carbon isoprenoid, which has commercial use in cosmetics and in vaccines. If it could be produced sustainably on a large scale, it could also be used instead of petroleum as a raw material for fuels and as feedstock for the chemical industry. The unicellular cyanobacterium Synechocystis PCC 6803 possesses a gene, slr2089, predicted to encode squalene hopene cyclase (Shc), an enzyme converting squalene into hopene, the substrate for forming hopanoids. Through inactivation of slr2089 (shc), we explored the possibility to produce squalene using cyanobacteria. The inactivation led to accumulation of squalene, to a level over 70 times higher than in wild type cells, reaching 0.67 mg OD750(-1) L(-1). We did not observe any significant growth deficiency in the Δshc strain compared to the wild type Synechocystis, even at high light conditions, suggesting that the observed squalene accumulation was not detrimental to growth, and that formation of hopene by Shc is not crucial for growth under normal conditions, nor for high-light stress tolerance. Effects of different light intensities and growth stages on squalene accumulation in the Δshc strain were investigated. We also identified a gene, sll0513, as a putative squalene synthase in Synechocystis, and verified its function by inactivation. In this work, we show that it is possible to use the cyanobacterium Synechocystis to generate squalene, a hydrocarbon of commercial interest and a potential biofuel. We also report the first identification of a squalene hopene cyclase, and the second identification of squalene synthase, in cyanobacteria.

Project description:Cyanobacteria are promising industrial platforms owing to their ability to produce diverse natural secondary metabolites and nonnative value-added biochemicals from CO2 and light. To fully utilize their industrial potency, it is critical to understand their photosynthetic efficiency under various environmental conditions. In this study, we elucidated the inhibitory mechanisms of photosynthesis under high-light and low-temperature stress conditions in the model cyanobacterium Synechocystis sp. PCC 6803. Under each stress condition, the transcript abundance and translation efficiency were measured using transcriptome sequencing (RNA-seq) and ribosome profiling, and the genome-wide transcription unit architecture was constructed by data integration of transcription start sites and transcript 3'-end positions obtained from differential RNA-seq and sequencing of 3'-ends (Term-seq), respectively. Our results suggested that the mode of photosynthesis inhibition differed between the two stress conditions; high light stress induced photodamage responses, while low temperature stress impaired the translation efficiency of photosynthesis-associated genes. In particular, poor translation of photosystem I resulted from ribosome stalling at the untranslated regions, affecting the overall photosynthetic yield under low temperature stress. Our comprehensive multiomics analysis with transcription unit architecture provides foundational information on photosynthesis for future industrial strain development. IMPORTANCE Cyanobacteria are a compelling biochemical production platform for their ability to propagate using light and atmospheric CO2 via photosynthesis. However, the engineering of strains is hampered by limited understanding of photosynthesis under diverse environmental conditions such as high-light and low-temperature stresses. Herein, we decipher the transcriptomic and translatomic responses of the photosynthetic efficiency to stress conditions using the integrative analysis of multiomic data generated by RNA-seq and ribosome profiling, respectively. Through the generated massive data, along with the guide of the genome-wide transcription unit architecture constructed by transcription start sites and transcript 3'-end positions, we identified the factors affecting photosynthesis at transcription, posttranscription, and translation levels. Importantly, the high-light stress induces photodamage responses, and the low-temperature stress cripples the translation efficiency of photosynthesis-associated genes. The resulting insights provide pivotal information for future cyanobacterial cell factories powered by the engineering toward robust photosynthesis ability.

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Influence of Chemically Disrupted Photosynthesis on Cyanobacterial Thylakoid Dynamics in Synechocystis sp. PCC 6803.

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