Rapid colour changes in <i>Euglena sanguinea</i> (Euglenophyceae) caused by internal lipid globule migration

The accumulation of red pigments, frequently carotenoids, under chronic stress is a response observed in diverse kinds of eukaryotic photoautotrophs. It is thought that red pigments protect the chlorophyll located underneath by a light-shielding mechanism. However, the synthesis or degradation of carotenoids is a slow process and this response is usually only observed when the stress is maintained over long periods of time. In contrast, rapid colour changes have been reported in the euglenophyte <i>Euglena sanguinea</i>. Here we study the ecophysiological process behind this phenomenon through chlorophyll fluorescence, and pigment, colour and ultrastructural analyses. Reddening in <i>E. sanguinea</i> was due to the presence of a large amount of free and esterified astaxanthin (representing 80% of the carotenoid pool). The process was highly dynamic, shifting from green to red in 8 min (and vice-versa in 20 min). This change was not due to <i>de novo</i> carotenogenesis, but to the relocation of cytoplasmic lipid globules where astaxanthin accumulates. Thus, red globules were observed to migrate from the centre of the cell to peripheral locations when exposed to high light. Globule migration seems to be so efficient that other classical photoprotective mechanisms are not operative in this species. Despite the presence and operation of the diadino-diatoxanthin cycle, non-photochemical quenching was almost undetectable. Since <i>E. sanguinea</i> forms extensive floating colonies, reddening can be observed at a much greater scale than at the cellular level and the mechanism described here is one of the fastest and most dramatic colour changes attributable to photosynthetic organisms at cell and landscape level. In conclusion <i>E. sanguinea</i> shows an extremely dynamic and efficient photoprotective mechanism, based more on organelle migration than on carotenoid biosynthesis, which prevents excess light absorption by chlorophylls reducing the need for other protective processes related to energy dissipation.长期胁迫下红色色素（多为类胡萝卜素（carotenoids））的积累，是多种真核光合自养生物中普遍存在的响应机制。学界普遍认为，这类红色色素可通过遮光（light-shielding）机制保护其下方的叶绿素（chlorophyll）。然而，类胡萝卜素的合成与降解过程较为缓慢，因此该响应通常仅在胁迫持续较长时间后才会显现。与之相对，眼虫门（euglenophyte）物种血红眼虫（*Euglena sanguinea*）被报道可发生快速的颜色变化。本研究通过叶绿素荧光（chlorophyll fluorescence）、色素组成、颜色变化及超微结构（ultrastructural）分析，探究该现象背后的生态生理过程。血红眼虫的变红现象源于大量游离型与酯化型虾青素（astaxanthin）的积累，该类物质占细胞类胡萝卜素总库的80%。该过程具有极强的动态性：可在8分钟内由绿色转变为红色，仅需20分钟即可恢复绿色。该颜色变化并非源于类胡萝卜素的从头生物合成（de novo carotenogenesis），而是源于虾青素积累所在的细胞质脂滴的重新定位。因此，当暴露于高光环境时，红色脂滴会从细胞中央迁移至外周区域。脂滴迁移的效率极高，以至于该物种无法激活其他经典的光保护（photoprotective）机制。尽管该物种拥有双甲藻黄素-硅藻黄素循环（diadino-diatoxanthin cycle）并可正常运作，但几乎无法检测到非光化学淬灭（non-photochemical quenching）现象。由于血红眼虫可形成大面积漂浮菌落，其变红现象可在远超单细胞尺度的范围内被观测到；本文所描述的机制，是光合生物在单细胞及景观尺度上已知的最快且最显著的颜色变化之一。综上，血红眼虫拥有一套极为动态且高效的光保护机制：该机制更依赖细胞器迁移而非类胡萝卜素生物合成，可阻止叶绿素吸收过量光能，从而降低了与能量耗散相关的其他保护过程的需求。