Modulation of the xanthophyll cycle improves biomass productivity and light tolerance of the microalga Nannochloropsis oceanica

Microalgae in photobioreactors encounter highly diverse light conditions along the culture depth because of cellular self-shading. Culture mixing also causes individual cells to rapidly shift from darkness to strong illumination, causing oversaturation of the photosynthetic apparatus and damage. Moreover, travelling from high light to darker layers can lead to energy loss through photoprotective mechanisms that remain active even when not needed. In the microalga Nannochloropsis oceanica the xanthophyll cycle plays a central role in the regulation of light harvesting and photoprotection, making it a central target for the optimization of photosynthetic performances in photobioreactors. Recently, we showed that the genetic control of the accumulation of enzymes that regulate the xanthophyll cycle, violaxanthin de-epoxidase (VDE), and zeaxanthin epoxidase (ZEP), can dramatically accelerate its kinetics. In this study, we characterized the impact of VDE and ZEP on the growth of N. oceanica. We monitored biomass productivity, pigment content, and photosynthetic performances, comparing single with double overexpressors in limiting and excess light conditions, in both tubular and flat panel photobioreactor systems. The acceleration of the xanthophyll cycle activation by increased accumulation of VDE led to increased photoprotection and enhanced light tolerance, but also excessive energy dissipation in limiting light. The enhancement of the xanthophyll cycle relaxation through ZEP accumulation, instead, reduced energy losses but could also increase photosensitivity. The combination of the two approaches resulted in the greatest benefit, leading to an improved productivity across different photobioreactor geometries and light conditions.