Rapid colour changes in Euglena sanguinea (Euglenophyceae) caused by internal lipid globule migration

The accumulation of red pigments under chronic stress is a response observed in most groups of oxygenic photoautotrophs. It is thought that the red pigments in the cell shield the chlorophyll located underneath from the light. Among these red pigments, the accumulation of carotenoids is one of the most frequent cases. However, the synthesis or degradation of carotenoids is a slow process and this response is usually only observed when the stress is maintained over a period of time. In the Euglenophyte Euglena sanguinea, this is due to the accumulation of a large amount of free and esterified astaxanthin (representing 80% of the carotenoid pool). While reddening is a slow and sometimes irreversible process in other phototrophs, reducing the efficiency of light harvesting by chlorophyll, in E. sanguinea it is highly dynamic, capable of shifting from red to green (and vice-versa) in 10-20 min. This change is not due to de novo carotenogenesis, but to the relocation of cytoplasmic lipid globules where astaxanthin accumulates. Thus, red globules migrate from the centre of the cell to peripheral locations when photoprotection is demanded. This protective system seems to be so efficient that other classical mechanisms are not operative in this species. For example, despite the presence and operation of the diadino-diatoxanthin cycle, nonphotochemical quenching (NPQ) is almost undetectable. Since E. sanguinea forms extensive floating colonies, reddening can be observed at much greater scale than at a cellular level, the mechanism described here being one of the fastest and most dramatic colour changes attributable to photosynthetic organisms at cell and landscape level. In sum, these data indicate an extremely dynamic and efficient photoprotective mechanism based on organelle migration more than on carotenoid biosynthesis that prevents excess light absorption by chlorophylls reducing the need for other protective processes related to energy dissipation.This work was supported by the Basque Government [UPV/EHU-GV IT-1018-16] [UPV/EHU PPG17/67 – GV IT-1040-16], and by the Spanish Ministry of Economy and Competitiveness (MINECO) and the European Research and Development Foundation (FEDER) through (i) [CTM2014-53902-C2-2-P] national grant and (ii) a “Juan de la Cierva-Incorporación” postdoctoral grant [IJCI-2014-22489] to BFM