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

Abstract 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 CO 2 -fixing pyrenoid) of the symbiotic microalga Micractinium conductrix significantly expands inside their host (the ciliate Paramecium 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. Significance statement Symbiotic interactions between a heterotrophic host and intracellular microalgae are widespread in aquatic ecosystems and are considered to be energized by the photosynthetically-derived carbon energy. However, little is known on the impact of symbiosis on the algal bioenergetics (e.g. carbon production and storage). This study reveals the morphological and physiological changes of a microalga inside a host at the subcellular scale over the day. We show that the photosynthetic machinery expands and carbon fixation and storage are boosted in symbiotic microalgae beyond their growth needs. This high photosynthetic production is very likely enhanced by the host energetic demands. Our findings advance our basic understanding of photosymbiosis and open new perspectives on the mechanisms and drivers of metabolic exchange between partners.