Modulation of xanthophyll cycle impacts biomass productivity in the marine microalgaNannochloropsis

Abstract

Life on earth depends on photosynthetic primary producers that exploit sunlight to fix CO2 into biomass. Approximately half of global primary production is associated with microalgae living in aquatic environments. Microalgae also represent a promising source of biomass to complement crop cultivation, and they could contribute to the development of a more sustainable bioeconomy. Photosynthetic organisms evolved multiple mechanisms involved in the regulation of photosynthesis to respond to highly variable environmental conditions. While essential to avoid photodamage, regulation of photosynthesis results in dissipation of absorbed light energy, generating a complex trade-off between protection from stress and light-use efficiency. This work investigates the impact of the xanthophyll cycle, the light-induced reversible conversion of violaxanthin into zeaxanthin, on the protection from excess light and on biomass productivity in the marine microalgae of the genus Nannochloropsis. Zeaxanthin is shown to have an essential role in protection from excess light, contributing to the induction of Non-Photochemical Quenching and scavenging of reactive oxygen species. On the other hand, the overexpression of Zeaxanthin Epoxidase, enables a faster re-conversion of zeaxanthin to violaxanthin that is shown to be advantageous for biomass productivity in dense cultures in photobioreactors. These results demonstrate that zeaxanthin accumulation is critical to respond to strong illumination, but it may lead to unnecessary energy losses in light-limiting conditions, and accelerating its re-conversion to violaxanthin provides an advantage for biomass productivity in microalgae.

Both major xanthophyll cycles present in nature can provide Non-Photochemical Quenching in the model diatomPhaeodactylum tricornutum

“…3 ). Similarly, ZEP inactivation under extreme irradiances has been postulated in Nannochloropsis gaditana , an heterokont displaying only the Vx cycle (77). We therefore conclude that in P. tricornutum ZEP3 is active exclusively under non-saturating irradiances to rapidly tune down NPQ, while ZEP2 has properties closer to the ZEP of higher plants and green algae, i.e., a constant activity under all irradiance condition (including darkness and HL) (45, 48, 49, 78).…”

Identifying the gene responsible for NPQ reversal inPhaeodactylum tricornutum

“…So, fast transitions from excess light to low light may result in lower light harvesting capacity due to the persistence of NPQ. Indeed, work in cyanobacteria and plants has shown that the deletion of NPQ capacity (Peers 2015) or tuning of NPQ induction and relaxation can lead to increased biomass accumulation in agricultural situations or dense algal cultures (Kromdijk et al, 2016;De Souza et al, 2022;Perin et al, 2023). We investigated if the level of NPQ could be tuned in Phaeodactylum using a synthetic promoter system.…”

Understanding regulation in complex environments: a route to enhance photosynthetic light-reactions in microalgae photobioreactors

“…As an example, the full activation of photoprotection takes some minutes in Nannochloropsis (Perin et al, 2023) and thus microalgae cells moving from the inner, light-limited, layers of photobioreactors to the most external, light-saturated, regions on a milliseconds/ seconds timeframe can experience light damage (Figure 4A).…”