Cho Sang-Hyeok, Jeong Yujin, Hong Seong-Joo, Lee Hookeun, Choi Hyung-Kyoon, Kim Dong-Myung, Lee Choul-Gyun, Cho Suhyung, Cho Byung-Kwan
Department of Biological Sciences, Korea Advanced Institute of Science and Technologygrid.37172.30, Daejeon, Republic of Korea.
Department of Biological Engineering, Inha University, Incheon, Republic of Korea.
mSystems. 2021 Dec 21;6(6):e0094321. doi: 10.1128/mSystems.00943-21. Epub 2021 Dec 7.
Cyanobacteria are promising industrial platforms owing to their ability to produce diverse natural secondary metabolites and nonnative value-added biochemicals from CO 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 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. Cyanobacteria are a compelling biochemical production platform for their ability to propagate using light and atmospheric CO 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.
蓝藻是很有前景的工业平台,因为它们能够利用二氧化碳和光能产生多种天然次生代谢产物和非天然的增值生化物质。为了充分发挥其工业潜力,了解它们在各种环境条件下的光合效率至关重要。在本研究中,我们阐明了模式蓝藻集胞藻PCC 6803在高光和低温胁迫条件下光合作用的抑制机制。在每种胁迫条件下,使用转录组测序(RNA-seq)和核糖体谱分析来测量转录本丰度和翻译效率,并通过分别从差异RNA-seq和3'端测序(Term-seq)获得的转录起始位点和转录本3'端位置的数据整合,构建全基因组转录单元结构。我们的结果表明,两种胁迫条件下光合作用的抑制模式不同;高光胁迫诱导光损伤反应,而低温胁迫损害光合作用相关基因的翻译效率。特别是,光系统I的翻译不佳是由于核糖体在非翻译区停滞所致,影响了低温胁迫下的整体光合产量。我们对转录单元结构的全面多组学分析为未来工业菌株的开发提供了光合作用的基础信息。蓝藻因其能够通过光合作用利用光和大气中的二氧化碳进行繁殖,是一个引人注目的生化生产平台。然而,由于对高光和低温胁迫等不同环境条件下的光合作用了解有限,菌株工程受到了阻碍。在此,我们分别利用RNA-seq和核糖体谱分析产生的多组学数据进行综合分析,解读光合效率对胁迫条件的转录组和翻译组反应。通过生成的大量数据,以及由转录起始位点和转录本3'端位置构建的全基因组转录单元结构的指导,我们在转录、转录后和翻译水平上确定了影响光合作用的因素。重要的是,高光胁迫诱导光损伤反应,低温胁迫削弱了光合作用相关基因的翻译效率。由此产生的见解为未来通过工程化实现强大光合能力的蓝藻细胞工厂提供了关键信息。