Sweet and fatty symbionts: photosynthetic productivity and carbon storage boosted in microalgae within a host

Symbiosis between a host and intracellular eukaryotic microalgae is a widespread life strategy in aquatic ecosystems. This partnership is considered to be mainly energized by the photosynthetically-derived carbon energy of microalgal symbionts. A major question is whether microalgae increase their photosynthetic production and decrease carbon storage in order to maximize carbon translocation to their host. By combining three-dimensional subcellular imaging and physiological analyses, we show that the photosynthetic machinery (chloroplast and CO₂-fixing pyrenoid) of the symbiotic microalgaMicractinium conductrixsignificantly expands inside their host (the ciliateParamecium bursaria) compared to the free-living state. This is accompanied by a 13-fold higher quantity of Rubisco enzymes and 16-fold higher carbon fixation rate. Time-resolved subcellular imaging revealed that photosynthetically-derived carbon is first allocated to starch during the day, with five times higher production in symbiosis despite low growth. Nearly half of the carbon stored in starch is consumed overnight and some accumulates in lipid droplets, which are 20-fold more voluminous in symbiotic microalgae. We also show that carbon is transferred to the host and hypothesize that much of this is respired by the high density of surrounding host mitochondria. We provide evidence that the boosted photosynthetic production of symbiotic microalgae could be explained by the energetic demands of the host. Overall, this study provides an unprecedented view of the subcellular remodeling and dynamics of carbon metabolism of microalgae inside a host, highlighting the potentially key role of the source-sink relationship in aquatic photosymbiosis.