The Control of Carbon Translocation in a Sea Anemone-Dinoflagellate Symbiosis from New Zealand

Anthopleura aureoradiata, a common sea anemone of New Zealand's intertidal mudflats and rocky shores, hosts symbiotic dinoflagellates of the genus Symbiodinium. This study investigated the control of photosynthetic carbon translocation in this symbiosis, and in particular the presence and operation of socalled 'host release factor' (HRF). Evidence for HRF exists in a number other algalinvertebrate symbioses, where tissue extracts of the host stimulate carbon release by isolated algal symbionts. However, its identity remains elusive and it has never been studied before in A. aureoradiata. Translocation of photosynthetically-fixed carbon in the intact symbiosis and in the presence of host tissue extract was measured using a 14C label. Zooxanthellae in the intact symbiosis released around 40% of their photosynthetically-fixed carbon to the anemone. Isolated zooxanthellae, however, translocated only 8%, even less than the amount of photosynthate liberated by zooxanthellae in FSW alone (11%). Photosynthetic rates per algal cell were similar in the intact symbiosis and both host homogenate and FSW incubations, meaning that the total amount of photosynthetically-fixed carbon released (in pg C/cell/h) by the zooxanthellae in these different situations reflected the %translocation values. Given the failure of homologous zooxanthellae (i.e. those from A. aureoradiata) to respond to homogenized host tissue, it was tested whether zooxanthellae from other host species (i.e. cultured heterologous algae) responded. Heterologous zooxanthellae representing 5 clades (A-E) of Symbiodinium were incubated in host tissue homogenate and photosynthate release again measured with 14C. The %translocation varied from 12-51% in A. aureoradiata homogenate and 17-67% in FSW, again suggesting a lack of an active HRF in the homogenized tissues of this sea anemone. Photosynthetic rates amongst the different heterologous algae also varied widely with, for instance, freshly isolated zooxanthellae from A. aureoradiata having 6-fold higher photosynthetic rates than cultured algae from the same clade (clade A). The zooxanthellae of A. aureoradiata are known to be N-sufficient in the field, and studies with other species have demonstrated that N-deficient zooxanthellae release more photosynthate in response to HRF than do N-sufficient ones. Therefore, induction of an HRF effect was attempted by starving sea anemones, and hence their zooxanthellae, prior to incubation of freshly isolated zooxanthellae in homogenized tissue. However, even after 8 weeks of starvation, the zooxanthellae showed no signs of N-deficiency (as indicated by the extent to which ammonium enhanced the rate of dark 14C fixation), meaning that the relationship with HRF activity could not be examined. The ability of these temperate zooxanthellae to maintain their Nsufficiency, even after relatively long periods of food deprivation, may indicate a lower reliance on host feeding for nitrogen than is seen in tropical zooxanthellae, or a greater capacity to use internal stores of nitrogen. The lack of photosynthate release by both homologous and heterologous zooxanthellae in host homogenate, as opposed to substantial carbon released in the intact symbiosis, suggests that control of carbon translocation in A. aureoradiata is not related to the activity of an HRF; alternatively, if an HRF is present, its activity is hindered when the symbiosis is disrupted. Further study is needed to determine what is responsible for the control of photosynthate translocation in the A. aureoradiata-Symbiodinium symbiosis