Metabolic interdependence and rewiring in radiolaria-microalgae photosymbioses

Marine planktonic Radiolaria harboring symbiotic microalgae are ubiquitous in the oceans and abundant in oligotrophic areas. In these low-nutrient environments, they are among the most important primary producers. Systematic studies of radiolarian biology are limited because radiolaria are non-culturable and prone to damage during sampling. To obtain insight into the mechanistic basis of radiolarian photosymbiosis, we address here the metabolic contributions of the partners to the performance of the holobiont. Therefore, we describe the metabolic inventory of two highly abundant photosymbiotic radiolaria-colony-forming Collodaria and single-celled Acantharia and compare their metabolomes to metabolomes of respective free-living algae. Most of the metabolites detected in the symbiosis are not present in the free-living algae, suggesting a significant transformation of symbionts' metabolites by the host. The metabolites identified in the holobiont and the free-living algae encompass molecules of primary metabolism and a number of osmolytes, including dimethylsulfoniopropionate. Mass spectrometry imaging revealed the presence of dimethylsulfoniopropionate in the symbionts and host cells, indicating that the algae provide osmolytic protection to the host. Furthermore, our findings suggest a possible dependence of Collodaria on symbiotic vitamin B3. Distinctive differences in phospholipid composition between free-living and symbiotic stages indicate that the algal cell membrane may undergo rearrangement in the symbiosis. Our results demonstrate a strong interdependence and rewiring of the algal metabolism underlying radiolaria-microalgae photosymbioses.