Impacts of Environmental Changes on the Use of Cellular Storage Products in a Temperate Cnidarian-Dinoflagellate Symbiosis

Abstract

Members of the phylum Cnidaria, such as corals and sea anemones, often form mutualistic endosymbiotic relationships with photosynthetic dinoflagellates that are founded upon a reciprocal exchange of nutrients. In this exchange, the cnidarian host provides its symbionts with nutrients derived through respiration, heterotrophy, and the environment, while the symbionts provide their host with products of photosynthesis. The energy derived from this exchange is utilized for metabolism, growth, and reproduction; alternatively, it can be accumulated into storage bodies for use during nutritional shortages or stress. Cnidarian-algal symbioses can be found throughout the world and vary in their sensitivity to stress, with environmental changes playing a prominent role in inducing stress. Tropical cnidarian-dinoflagellate symbioses are particularly vulnerable to temperature change, with increases of just 1-2℃ above their upper thermal limit often resulting in bleaching (the breakdown of symbiosis via symbiont expulsion). In contrast, temperate cnidarian-dinoflagellate symbioses exhibit far greater tolerance to such environmental stressors, and are rarely seen to bleach in the field. It is unclear how temperate cnidarian-dinoflagellate symbioses achieve this resilience and stability.

This thesis examines the effects of changes in temperature and irradiance on the content of energy-rich cellular storage products in the temperate sea anemone Anthopleura aureoradiata and its dinoflagellate endosymbionts (family: Symbiodiniaceae), in order to assess the potential of these compounds in contributing to the overall stability of the symbiosis. In particular, symbiont density and chlorophyll content (as well as photosynthetic efficiency, for experimental study only), in addition to both symbiont and host protein content, served as indicators of physiological health, and were then related to the accumulation of cellular storage products such as lipids and carbohydrates.

A field study was conducted in which a population of A. aureoradiata was sampled from Wellington Harbor, New Zealand, at monthly intervals for one year. Despite monthly and seasonal variability in the physiological parameters measured, the symbiosis remained functional and stable (i.e. no signs of bleaching) throughout the year. The greatest inter-seasonal variation occurred in the symbiont cell-specific carbohydrate content, which decreased significantly between spring and summer. In contrast, host lipid content exhibited less variation than all other symbiont and host storage products. These observations suggest that symbiont carbohydrate stores are primarily utilized to sustain the symbiosis during times of seasonal environmental change (in this case, correlating with increased light and temperature during summer), while lipids may be kept in reserve. The robustness of this field population is expected; being a native species, A. aureoradiata is likely highly acclimated to the conditions that were observed throughout the year of this field study. A separate population of A. aureoradiata was subsequently acclimated to a moderate regime of temperature and irradiance, and then exposed to one of six treatments of different combined temperatures and irradiances (based on seasonal conditions in the Wellington Harbour), to establish their interactive effects on cellular storage product content. Specifically, three thermal regimes (low: 9±1°C, moderate: 14.5±1°C, high: 21±1°C), each at a low (70±10 µmol photons m-2 s-1) or high (145±15 µmol photons m-2 s-1) irradiance, were maintained for a total of sixteen weeks. Unlike in the field, a breakdown in symbiosis was observed; photo-physiological dysfunction of the symbiosis was observed within four weeks in all anemones exposed to low temperature at both irradiances, and bleaching was apparent by week eight. This response likely arose from a combination of the rapid decrease in temperature experienced upon distribution into the low-temperature tank, as well as the prolonged nature of the conditions in the experiment, which would not be experienced in the field. In contrast, the anemones maintained at both irradiances in the moderate and high temperature treatments maintained a stable symbiosis, suggesting that these conditions were not extreme enough to cause notable stress. In fact, anemones kept under both low and high irradiance within the moderate temperature treatment increased in symbiont density and exhibited the highest host lipid content relative to the other treatments, suggesting that this treatment was near-optimal for the symbiosis. Perhaps interestingly, both the moderate and high temperature treatments induced significant reductions in symbiont-specific protein, lipid, and carbohydrate content, while host storage products decreased less drastically. This observation suggests increased utilization of symbiont storage products to maintain a healthy symbiosis under these experimental conditions.

My findings are consistent with previous reports of seasonal stability in temperate cnidarian-dinoflagellate symbioses; moreover, I provide experimental evidence for the utilization of symbiont storage products as a means of maintaining symbiosis stability, though this was less apparent in the field. Although recent studies have made great progress in identifying patterns of stability in temperate cnidarian-dinoflagellate symbioses, additional studies are required to build a more comprehensive picture of the mechanisms involved. Future studies would benefit from increased frequency of field sampling, including assessments of nutrient availability and host reproductive cycles, to better understand the monthly and seasonal variability in the intracellular storage product use observed in the field. Nevertheless, results of this study contribute to an improved understanding of the physiology and remarkable stability of temperate cnidarian-dinoflagellate symbioses, with implications for predictions of how they might respond to future climate change scenarios.