Metabolite comparisons and the identity of nutrients translocated from symbiotic algae to an animal host

Abstract

SUMMARYDinoflagellate algae of the genus Symbiodinium in symbiosis with marine animals release much of their photosynthetic carbon to the animal host. The compounds translocated to the host (`mobile compounds') were investigated by metabolite comparison as follows: a substrate was identified as a candidate mobile compound when comparable profiles of metabolites were generated from host metabolism of this substrate (supplied exogenously) and the endogenous mobile compounds. When the sea anemone Anemonia viridis was incubated with NaH14CO2 under photosynthesizing conditions, most of the radioactivity in the animal tissue was recovered from the low-molecular-mass fraction and distributed in the ratio 1:2:1 between the neutral, acidic and basic sub-fractions. Prominent 14C-labelled compounds included glucose, malate and glucose-6-phosphate. When the symbiosis was incubated with 14C-labelled glucose plus succinate or fumarate(but none of eight other substrate combinations tested), the 14C-labelled metabolites closely matched those obtained with NaH14CO2. These data suggest that glucose and succinate/fumarate (or metabolically allied compounds) may be important photosynthetic compounds transferred from the Symbiodinium cells to the tissues of A. viridis. Metabolite comparisons can be applied to study nutritional interactions in symbioses involving photosynthetic algae and, with appropriate modification, other associations between microorganisms and plants or animals.

Experimentally Induced Bleaching in the Sea Anemone Exaiptasia Supports Glucose as a Main Metabolite Associated with Its Symbiosis

“…The consistency of our results with the literature [13,36,45] strongly supports the hypothesis that glucose is a major chemical form in the translocation of reduced carbon in the symbiosis of E. pallida. The possibility of glucose being synthesized from glycerol seems unlikely, being an energyconsuming path.…”

Metabolite profiling of symbiont and host during thermal stress and bleaching in a model cnidarian-dinoflagellate symbiosis

“…Secondly, we also detected accumulations in symbiont pools of numerous other amino acid groups; these included isoleucine and valine, which, under functional conditions, are thought to be synthesised by the symbiont and translocated to the host (Wang and Douglas, 1999). Accumulations of these amino acids are therefore once again likely to be indicative of a reduction in the activity of ATP-consuming biosynthesis pathways, such as transamination and protein synthesis and of declines in downstream mobile product translocation to the host, coupled to increases in ATP-generating pathways such as the breakdown of proteins during gluconeogenesis (Wang and Douglas, 1998;Whitehead and Douglas, 2003).…”

Evidence that glucose is the major transferred metabolite in dinoflagellate–cnidarian symbiosis

“…Some earlier studies also detected glucose as an apparently transferred metabolite in dinoflagellate-cnidarian symbiosis. Notably, in a careful study in which intact Anemonia viridis anemones were labeled with 14 Cbicarbonate, Whitehead and Douglas found glucose and several other small molecules as prominently labeled metabolites in the host tissue (Whitehead and Douglas, 2003). Glucose also appears to be the major compound released by Symbiodinium to the host in the undisturbed dinoflagellate-giant-clam symbiosis (Ishikura et al, 1999).…”

“…However, Ishikura and co-workers did detect labeled glycerol when dinoflagellates freshly isolated from the clams were exposed to host homogenate or when the host mantle was damaged, even though exogenously supplied labeled glycerol was not converted rapidly to glucose in the amounts seen in the intact system (Ishikura et al, 1999). Similarly, when the anemone Anemonia viridis was fractionated after labeling the intact holobiont, the host fraction was found to contain 14 C-labeled amino acids, glucose, malate, succinate and fumarate, but no detectable glycerol (Whitehead and Douglas, 2003). Taken together, these studies have raised the possibility that glycerol production and/or release is linked to damage to the symbiotic systems rather than being integral to the intact symbiosis.…”