Metabolic partitioning between photosynthesis and osmotrophy in Collodaria photosymbiotic holobionts

Collodaria (Radiolaria) are widespread marine planktonic protists that host photosynthetic microalgal symbionts. Within this photosymbiosis, they can contribute substantially to primary production, particularly in oligotrophic ocean regions. Despite their ecological importance, the mechanisms underlying the formation and maintenance of photosymbiosis are poorly understood. To uncover the metabolic dependencies within this photosymbiotic system, we develop a stable isotope labeling strategy that allows us to investigate the assimilation of inorganic and organic carbon in the Collodaria holobiont. By integrating metabolomic profiling with isotopic labeling analyses, we demonstrate that algal photosynthesis makes a substantial contribution to the holobiont carbohydrate pool. In particular, we observe the incorporation of inorganic carbon into glucose and fructose, followed by the enrichment of other metabolites including ribose. In contrast, osmotrophic uptake of dissolved organic compounds derived from labeled algal lysate does not lead to the incorporation of any of these carbohydrates, suggesting no significant contribution of osmotrophy to the holobiont's carbohydrate pool. In contrast, specialized metabolites, such as dimethylsulfoniopropionate (DMSP) and betaines, are primarily acquired through osmotrophy implying a minor contribution of photosymbionts. Our findings thus reveal defined roles of phototrophic and osmotrophic metabolism in the Collodaria holobiont with consequences for our understanding of element fluxes in plankton.