The importance and movement of mud bacterial carbon within the symbiosis of the New Zealand sea anemone Anthopleura aureoradiata
Authors:   , Cornwall Andrew 
Published: November 2021

<p>A. aureoradiata is New Zealand’s only native cnidarian to form a phototrophic symbiosis with dinoflagellate microalgae. It is of particular interest as it can be found in estuarine mudflat habitats attached to cockles, where it spends a portion of the day submerged under the mud, either partially or completely. This scenario is very different to the situation in the tropics, where comparable symbioses (e.g. those with reef-building corals) live in brightly lit, clear waters. How A. aureoradiata maintains a stable symbiosis is therefore of considerable interest, with one potential mechanism involving the acquisition of carbon from the surrounding mud to counter the reduced availability of light and hence the reduced rate of photosynthesis.  In this thesis, I established the extent to which organic carbon in mud (especially bacteria) can be assimilated by A. aureoradiata and to what extent, if any, this carbon contributes to symbiosis nutrition and facilitates symbiosis stability under otherwise sub-optimal conditions. In the first instance, anemones were given access to¹³C glucose-labelled mud for 12 hours, in both the light and dark, and the extent of label incorporation (¹³C enrichment) in both the host and symbiont was measured by mass spectrometry. Subsequently, A. aureoradiata was starved of planktonic food for six weeks in the presence of differing quantities of unlabelled mud (‘no-mud’, ‘low-mud’ and ‘high-mud’), either with or without light, and a range of nutritional and biomass parameters measured. These included symbiont density, host protein content, and the accumulation of host lipid and symbiont starch stores.  Both the host anemone and its symbiotic algae showed signs of ¹³C uptake from the mud. Host anemones maintained in the dark assimilated more ¹³C label from the mud than did anemones incubated in the light, while the extent of label assimilation by the symbionts was unaffected by irradiance. Enhanced heterotrophic feeding in the dark is consistent with patterns reported for other symbiotic cnidarians, such as reef corals, where the host must counter the reduced availability of photosynthate from the symbiotic algae. However, the reason for the equal labelling of the symbionts in the light and dark is less clear. Nevertheless, factors such as reverse translocation in the dark (i.e. the transfer of organic carbon from host to symbiont), dark fixation of inorganic carbon, and a higher respiration rate of symbionts in the light than dark, could act either alone or in concert to produce the labelling pattern seen.  While the host and symbiont showed evidence of carbon uptake from the surrounding mud, mud quantity had no effect on either the host’s or symbiont’s storage products (% of starch in symbiont biomass, host protein content and lipid content), or on symbiont density. The lack of an effect of mud suggests that mud-derived bacteria comprise little of the host’s natural diet. In contrast, increased light availability (independent of mud availability) did lead to elevated symbiont density and symbiont starch content, consistent with the phototrophic nature of this symbiosis. More surprising was that host protein content was highest in the dark, suggesting perhaps that the symbionts were less of an energetic drain on their host when starved in the dark due to their lower population density.  In summary, my thesis provides evidence that A. aureoradiata and its symbiotic algae can use organic carbon obtained from the surrounding mud for their nutrition, but that this carbon source is of only negligible importance. These results are consistent with previous findings for the uptake and role of mud-derived nitrogen in this system. Further work to establish how this symbiosis maintains its remarkable stability under apparently sub-optimal, low-light conditions is therefore needed.</p>