Heterotrophy and symbiosis affect energy reserves for pedal lacerates in the sea anemone <i>Exaiptasia diaphana</i>

Nutrient exchange between corals and their dinoflagellate symbionts is the foundation of the stable symbiosis that underpins coral reef ecosystem success. The cnidarian-dinoflagellate holobiont engages in both autotrophy (photosynthates supplied by the symbiont) and heterotrophy (feeding by the host on microscopic organisms and particulate matter) to meet their nutritional demands. While considerable research has been devoted to understanding nutrient dynamics in adult corals and other symbiotic cnidarians, less is known about how the combination of heterotrophy and autotrophy influences nutrition within and across generations. We investigated the role of symbiosis and heterotrophy in the sea anemone <i>Exaiptasia diaphana</i> (commonly called Aiptasia), a model system for the study of coral symbiosis. We examined how different feeding regimens affected parental growth and how nutritional status of the adult influenced nutrition of asexual offspring (pedal lacerates). After one-month, heterotrophic feeding resulted in larger pedal disk sizes in aposymbiotic adults regardless of lighting. However, in symbiotic groups, a lack of heterotrophy and/or autotrophy resulted in almost no growth or a decrease in body size. This suggests that symbiosis incurs a cost on the host when it is deprived of multiple food sources, and that autotrophy needs to be paired with heterotrophy for significant growth to occur in symbiotic adults. In pedal lacerates, we found that heterotrophic feeding and symbiotic state have an interactive effect on metabolite abundance. Symbiotic lacerates with access to food and light had significantly greater carbohydrates compared to all other groups, suggesting that the symbionts require both to produce carbohydrates in high quantities. Lipid content varied by symbiotic state, with aposymbiotic lacerates having more total lipids, while symbiotic lacerates had more nutrient-rich neutral lipids, indicating that symbiosis alters the production and abundance of different lipid classes. Symbiosis and heterotrophy significantly increased total protein in lacerates. Our results show that the combination of heterotrophy and autotrophy greatly increases growth rate and the abundance of carbohydrates and protein in symbiotic cnidarians, but nutritional lipids only differ based on symbiotic state, which suggests that the symbionts greatly increase the overall metabolic pool of the holobiont. In addition, our results show that there is a cost to hosting symbionts when autotrophy and/or heterotrophy are removed. This highlights the importance of heterotrophy in the success of symbiotic cnidarians within and across generations.