Systematic identification of light-regulated cold-responsive proteome in a model cyanobacterium.

Differential expression of cold-responsive proteins is necessary for cyanobacteria to acclimate to cold stress frequently occurring in their natural habitats. Accumulating evidence indicates that cold-induced expression of certain proteins is dependent on light illumination, but a systematic identification of light-dependent and/or light-independent cold-responsive proteins in cyanobacteria is still lacking. Herein, we comprehensively identified cold-responsive proteins in a model cyanobacterium Synechocystis sp. PCC 6803 (Hereafter Synechocystis) that was cold-stressed in light or in dark. In total, 72 proteins were identified as cold-responsive, including 19 and 17 proteins whose cold-responsiveness are light-dependent and light-independent, respectively. Bioinformatic analysis revealed that outer membrane proteins, proteins involved in translation, and proteins involved in divergent types of stress responses were highly enriched in the cold-responsive proteins. Moreover, a protein network responsible for nitrogen assimilation and amino acid biosynthesis, transcription, and translation were upregulated in response to the cold stress. The network contains both light-dependent and light-independent cold-responsive proteins, probably for fine tuning its activity to endow Synechocystis the flexibility necessary for cold adaptation in their natural habitats, where days and nights are alternating. Together, our results should serve as an important resource for future study toward understanding the mechanism of cold acclimation in cyanobacteria.

SIGNIFICANCE: Photosynthetic cyanobacteria need to acclimate to frequently occurring abiotic stresses such as cold in their natural habitats, and the acclimation process has to be coordinated with photosynthesis, the light-dependent process that provides carbon and energy for propagation of cyanobacteria. It is conceivable that cold-induced differential protein expression can also be regulated by light. Hence it is important to systematically identify cold responsive proteins that are regulated or not regulated by light to better understand the mechanism of cold acclimation in cyanobacteria. In this manuscript, we identified a network involved in protein synthesis that were upregulated by cold. The network contains both light-dependent and light-independent cold-inducible proteins, presumably for fine tuning the activity of the network in natural habitats of cyanobacteria where days and nights are alternating. This finding underscores the significance of proteome reprograming toward enhancing protein synthesis in cold adaptation.