The Microalga Nannochloropsis during Transition from Quiescence to Autotrophy in Response to Nitrogen Availability

• Published in: Plant physiology (Bethesda) 2020-02, Vol.182 (2), p.819-839
• Main Authors: Zienkiewicz, Agnieszka, Zienkiewicz, Krzysztof, Poliner, Eric, Pulman, Jane A, Du, Zhi-Yan, Stefano, Giovanni, Tsai, Chia-Hong, Horn, Patrick, Feussner, Ivo, Farre, Eva M, Childs, Kevin L, Brandizzi, Federica, Benning, Christoph
• Format: Article
• Language: English
• Subjects: Autophagy - genetics; Autophagy - physiology; Autophagy-Related Protein 8 Family - metabolism; Autotrophic Processes - genetics; Autotrophic Processes - physiology; Cell Cycle - genetics; Cell Cycle - physiology; Cluster Analysis; Fatty Acids - biosynthesis; Fatty Acids - metabolism; Gene Expression Profiling; Gene Expression Regulation - genetics; Gene Expression Regulation - physiology; Gene Ontology; Homeostasis - genetics; Homeostasis - physiology; Lipid Droplets - metabolism; Lipid Droplets - ultrastructure; Lipid Metabolism - genetics; Lipid Metabolism - physiology; Microalgae - genetics; Microalgae - metabolism; Microscopy, Electron, Transmission; Multigene Family; Nitrogen - metabolism; Nutrigenomics; Photosynthesis - genetics; Photosynthesis - physiology; Stramenopiles - genetics; Stramenopiles - metabolism; Triglycerides - metabolism; Vacuoles - metabolism; Vacuoles - ultrastructure
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.19.00854

The marine microalgae (CCMP1779) is a prolific producer of oil and is considered a viable and sustainable resource for biofuel feedstocks. Nitrogen (N) availability has a strong impact on the physiological status and metabolism of microalgal cells, but the exact nature of this response is poorly understood. To fill this gap we performed transcriptomic profiling combined with cellular and molecular analyses of CCMP1779 during the transition from quiescence to autotrophy. N deprivation-induced quiescence was accompanied by a strong reorganization of the photosynthetic apparatus and changes in the lipid homeostasis, leading to accumulation of triacylglycerol. Cell cycle activation and re-establishment of photosynthetic activity observed in response to resupply of the growth medium with N were accompanied by a rapid degradation of triacylglycerol stored in lipid droplets (LDs). Besides observing LD translocation into vacuoles, we also provide evidence for direct interaction between the LD surface protein ( LDSP) and AUTOPHAGY-RELATED8 ( ATG8) protein and show a role of microlipophagy in LD turnover in CCMP1779. This knowledge is crucial not only for understanding the fundamental mechanisms controlling the cellular energy homeostasis in microalgal cells but also for development of efficient strategies to achieve higher algal biomass and better microalgal lipid productivity.