Osmoregulation and the Anthozoan-Dinoflagellate Symbiosis

This study investigated the responses of the temperate anemone Anthopleura aureoradiata, and the tropical coral Acropora aspera to osmotic stress and the role that free amino acids (FAAs) may play in the osmoregulatory mechanism of these anthozoan-dinoflagellate symbioses. Specimens were exposed to a range of hypo- and hyper-saline conditions for durations of 1, 12, 48 and 96 hours, whereupon respiration and photosynthetic rates were measured as physiological indicators of osmotic stress. High performance liquid chromatography was used to quantify 15 FAAs within the anthozoan host tissues to establish the response of FAA pools to osmotic stress and whether FAAs are used in an osmoregulatory capacity. Aposymbiotic specimens of A. aureoradiata were similarly tested to establish if the presence of symbiotic dinoflagellates alters the host’s capacity to respond to osmotic stress given that the symbionts are known to release FAAs into the host cytoplasm. In A. aureoradiata, significant changes in respiration were only observed with exposure to the extreme hypo-osmotic salinity of 12‰, with respiration decreasing by 67% after 1 hour of exposure. No significant changes in respiration were seen at 25, 43 or 50‰, despite a 52% decrease in respiration seen at the hyper-saline treatment of 50‰. The response of the coral A. aspera was markedly different, showing an increase in respiration in response to hypo-salinity (22 and 28‰). Interestingly, the most pronounced respiratory increase of up to 460% occurred in the less extreme hypo-saline treatment of 28‰. The response of photosynthesis also showed differences between the two species. In the symbiotic A. aureoradiata, photosynthesis declined by 61% after the 1 hour exposure to 12‰ and further decreased to 72% below control rates after 96 hours. While in A. aspera, photosynthesis showed no significant deviation from control levels at any of the treatment salinities. FAA pools in both A. aureoradiata and A. aspera showed significant responses to osmotic stress. In symbiotic A. aureoradiata, exposure to 12‰ caused total FAA pools to decline by 50% after 1 hour, after which a seemingly stable state was reached. A hyper-osmotic treatment of 50‰ resulted in a similar trend with a more than 50% decrease after 1 hour of exposure. In A. aspera, the response of the FAA pool was markedly different, with the concentration increasing by up to 200% with exposure to 22‰ and by more than 260% at 28‰. Interestingly, one on the main constituents of FAA pools in A. aureoradiata, Taurine (15% of FAA pools at 35‰), was not present in measurable quantities within A. aspera host tissue. In aposymbiotic individuals of A. aureoradiata exposed to extreme hypo- and hyper-saline treatments of 12 and 50‰ a significant impact on respiration was only observed at 12‰, with a 77% decrease in respiration after 96 hours. Changes in FAA pools of aposymbiotic A. aureoradiata were only seen after 12 hours exposure to 50‰ with a significant 26% decrease. However, the direct comparison between symbiotic and aposymbiotic A. aureoradiata did serve to highlight the contribution of symbiont-derived FAAs to the host pool of FAAs, with FAA pools in aposymbiotic anemones up to 41% lower than those found in symbiotic anemones. The results seen here were not suggestive of FAAs being regulated for the explicit use as compatible organic osmolytes. Rather, changes in FAA pools showed changes consistent with other stress responses. Moreover, the response of anthozoan-dinoflagellate symbioses to osmotic stress appears to be species specific, or at least taxa specific, as the responses of respiration, photosynthesis and FAA pools were very different between the temperate anemone A. aureoradiata and the tropical coral A. aspera. Nevertheless, differences in the respiratory response between symbiotic and apo-symbiotic anemones did indicate some influence of the dinoflagellate symbionts on the ability of the anthozoan host to mediate osmotic stress. It may therefore be that other symbiont-derived compounds are utilised as compatible organic osmolytes (COOs), with a primary candidate being glycerol. This warrants further investigation.