Host-Zooxanthella Interactions in Four Temperate Marine Invertebrate Symbioses: Assessment of Effect of Host Extracts on Symbionts

Abstract

Photosynthesis and translocation of photosynthetic products from symbiotic zooxanthellae in four species of temperate-latitude invertebrates were investigated in vivo and in vitro. In vivo, zooxanthellae fixed 14C and translocated a substantial proportion of fixed products to host tissues. In vitro, the effect of host tissue extracts on isolated zooxanthellae varied. Extracts of the soft coral Capnella gaboensis, lysed zooxanthellae after a relatively short exposure. Those of the zoanthid Zoanthus robustus and the nudibranch Pteraeolidia ianthina had little effect on translocation of organic carbon from zooxanthellae. In contrast, host extract of the scleractinian coral Plesiastrea versipora stimulated the release of up to 42% of the total 14C fixed, and the magnitude of release was positively correlated with the protein concentration of the extract. Host extracts had no effect on photosynthetic rates in algal symbionts. The effect of P. versipora extract on isolated zooxanthellae was studied. This extract caused zooxanthellae to divert photosynthetic products from lipid synthesis to the production of neutral compounds, principally glycerol, and these compounds were the predominant form of carbon detected extracellularly after incubating zooxanthellae in this extract. Only organic compounds made during the period of exposure of zooxanthellae to host extract, and not pre-formed photosynthetic products, were translocated. The translocation-inducing activity of host extract was almost completely destroyed by heating (100{deg}C), and a preliminary attempt to fractionate the tissue extract revealed that the active constituent did not pass through dialysis tubing of nominal pore size 10,000 D. These results are discussed in relation to host control of symbiotic partners, and to previous reports of "host-release factors" in other invertebrate symbioses.

Cultivating endosymbionts — Host environmental mimics support the survival of Symbiodinium C15 ex hospite

“…There is ample evidence that host homogenate can stimulate release of photosynthetic products from symbiotic algae of giant clams, anemones, zoanthids and corals (Cook and Davy, 2001;Gates et al, 1995;Grant et al, 1997;Ishikura et al, 2004;Sutton and Hoegh-Guldberg, 1990;Trench, 1971). While a beneficial effect appears to be only valid for symbiotic and not for aposymbiotic hosts (Trench, 1971), there is also evidence for adverse effects of certain host homogenates (e.g., Sutton and Hoegh-Guldberg, 1990).…”

“…While a beneficial effect appears to be only valid for symbiotic and not for aposymbiotic hosts (Trench, 1971), there is also evidence for adverse effects of certain host homogenates (e.g., Sutton and Hoegh-Guldberg, 1990). Host derived homogenate in synthetic seawater stabilized cell densities of freshly isolated Symbiodinium C15 cells over six to eight days and stimulated considerable proliferation in one of our trials.…”

How a host cell signalling molecule modifies carbon metabolism in symbionts of the coral Plesiastrea versipora

“…When algae from P. versipora were incubated in the light for 1 h with NaH 14 CO 3 minus HRF, followed by a 1-h chase period in the dark plus HRF, 4-11% of the recently fixed 14 C was released. This amount was not altered by HRF [2]. However, transfer of carbon from algal symbionts to the animal host in the dark may occur over a longer period.…”

“…The main 14 C-labelled compound released from freshly isolated Symbiodinium incubated in the light in homogenized P. versipora tissue with NaH 14 CO 3 is glycerol [2,3]. Release of glucose from P. versipora algae has not been observed [16,17].…”

“…The scleractinian coral Plesiastrea versipora (Lamarck 1816; Fig. 1A) regulates its endosymbionts via a host cell signalling molecule, termed host release factor (HRF) [2,3], that stimulates its algal symbionts to release products of photosynthesis (photosynthate), thus providing nutrients for the animal host [4]. P. versipora is a useful model for studying HRF, because it is a long-lived hard coral that is widely distributed throughout the tropical and temperate Indo-Pacific [5].…”