Heterotrophic dependence and bidirectional metabolite exchange dynamics in a temperate coral

In temperate ecosystems, where cold, turbid waters constrain symbiotic potential, corals have evolved facultative symbiosis, providing an opportunity to explore coral energetics in the face of global climate change. We conducted an in situ light exclusion experiment on the facultatively symbiotic temperate coral Astrangia poculata to explore the interactions among environmental variables and host-symbiont metabolism. Corals exhibited photophysiological plasticity and ecotype switching based on light environment. Symbiont density positively correlated with calice density, despite A. poculata's slow calcification rate. To quantify the trophic ecology of the host and symbionts, we conducted compound-specific stable isotope analysis of amino acids. Coral host essential amino acid carbon isotope fingerprints overlapped between ecotypes and among light treatments and were distinct from symbionts, indicating that photosynthetically derived metabolites were present but not translocated en masse from symbiont to host. Instead, coral hosts relied heavily on heterotrophic carbon sources. This is corroborated by high trophic positions of host (2.5 ± 0.1) and symbionts (2.4 ± 0.3), which were well above presumed “autotrophs,” and ΣV values greater than the nominal cut off for “microbially reworked organic matter” (> 1.5), indicating bidirectional metabolite exchange between host and symbionts. While light availability modulated photophysiology and morphology, trophic ecology was rigid across different light conditions and between symbiotic ecotypes. Our data suggest that A. poculata predominantly relies on heterotrophy and bidirectionally shares metabolites with their mixotrophic symbionts irrespective of light conditions, challenging the classic theory of metabolism and symbiosis in temperate corals.