Highly effective energy transfer in the autotroph-heterotroph symbiosis: insights from compound-specific isotope analysis of amino acids

<jats:title>Abstract</jats:title> <jats:p>Many species establish symbiotic partnerships with different organisms to benefit energetically from living together to fit into environments, and such symbiosis is frequently found in the modern ocean as well as throughout Earth’s history. For example, coral reef ecosystems represent one of the most productive and biologically diverse ecosystems in the modern ocean, which is simply explained by an assumption that many autotroph-heterotroph symbiotic species found in there increase the efficiency of trophic transfer from primary producers (i.e., algal symbionts) to primary consumers (i.e., animal hosts), and that such high efficiency may be propagated to entire food webs. However, this high efficiency has not been proved and illustrated with quantitative data in the trophic transfer of photosynthates from algal symbionts to animal hosts. In the present study, we measured the energetic balance between degradation and biomass growth, which is a major factor of the efficiency of trophic transfer, based on the analysis of stable nitrogen isotope ratios of amino acids for several species including sea anemones, stony corals, zoanthids, and soft corals, that were bred under an autotrophic condition in a laboratory aquarium. The results confirm that the symbiosis indeed provides highly effective energy transfer of algal photosynthates to animal hosts, and allow us to quantify that the energy transfer in the symbiosis increases by approximately twice of that when non-symbiotic herbivorous species feed on primary producers. These results induce a new perspective that the effective energy transfer driven by symbiosis is a critical factor controlling the development of highly productive and biologically diverse ecosystems in the modern ocean as well as throughout Earth’s history. </jats:p>