Acquisition of desiccation tolerance in Haematococcus pluvialis requires photosynthesis and coincides with lipid and astaxanthin accumulation

The unicellular Chlorophyte Haematococcus pluvialis synthesizes astaxanthin and lipids in response to various stress factors. This species colonises temporary water bodies, leaving it vulnerable to desiccation, but mechanisms of desiccation tolerance (DT) in H. pluvialis have not yet been explored. We found that astaxanthin-rich red-coloured H. pluvialis cells tolerated desiccation sensu stricto, but green-coloured cells did not. Mechanisms of DT were elucidated by studying cells under conditions that permitted or prevented attainment of DT. Cellular changes associated with attainment of DT included major reorganisation of cell ultra-structure, such as reduction of chloroplast area and synthesis of astaxanthin-rich lipid bodies. Such changes were prevented in cells desiccated in the dark, or in the light, by blocking electron transfer out of photosystem II. Processes occurring during acclimation to desiccation under low light overlapped with those under high light without desiccation, a treatment that also led to DT, e.g. fatty acids, lipid bodies, astaxanthin, α-tocopherol and glutathione accumulated under both treatments. Furthermore, exposing cells grown in liquid medium to a water-saturated atmosphere without any dehydration also enabled attainment of DT, but at a slower rate compared to when cells were dehydrated. We conclude that atmospheric exposure alone triggered acclimation to desiccation, and photosynthesis powered this process, but neither high light stress nor dehydration are strictly necessary.