Meta-analysis reveals host-dependent nitrogen recycling as a mechanism of symbiont control in Aiptasia

Abstract

The metabolic symbiosis with photosynthetic algae of the genus Symbiodinium allows corals to thrive in the oligotrophic environments of tropical seas. Many aspects of this relationship have been investigated using transcriptomic analyses in the emerging model organism Aiptasia. However, previous studies identified thousands of putatively symbiosis-related genes, making it difficult to disentangle symbiosis-induced responses from undesired experimental parameters. Using a meta-analysis approach, we identified a core set of 731 high-confidence symbiosis-associated genes that reveal host-dependent recycling of waste ammonium and amino acid synthesis as central processes in this relationship. Combining transcriptomic and metabolomic analyses, we show that symbiont-derived carbon enables host recycling of ammonium into nonessential amino acids. We propose that this provides a regulatory mechanism to control symbiont growth through a carbon-dependent negative feedback of nitrogen availability to the symbiont. The dependence of this mechanism on symbiont-derived carbon highlights the susceptibility of this symbiosis to changes in carbon translocation, as imposed by environmental stress.