Metabolic integration between symbiotic cyanobacteria and sponges: a possible mechanism

Metabolic relationships between symbiotic cyanobacteria and host sponge have been investigated in the marine species Chondrilla nucula and Petrosia ficiformis (collected in the Ligurian Sea in 1992). DNA, RNA, total protein, cytosolic protein, total sugar, cytosolic sugar, total lipid, nonprotein sulfhydryl groups, glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase were assayed in cortex-free sponge tissue, where cyanobacteria are all but absent. For both species, biochemical parameters were determined in specimens living in illuminated habitats and in dark caves, where sponges are virtually aposymbiotic for cyanobacteria. As C. nucula is unable to colonize dark sites, specimens of this species were artificially transferred to a cave and maintained in dark conditions for 6 mo. Results showed that in the absence of light (i.e., in the absence of cyanobacteria) C. nucula undergo metabolic collapse and thiol depletion. In contrast, P. ficiformis activates heterotrophic metabolism and mechanisms which balance the loss of cell reducing power. This suggests that cyanobacteria effectively participate in controlling the redox potential of the host cells by the transfer of reducing equivalents. Only P. ficiformis is capable of counteracting, by means of heterotrophic metabolism, the loss of the contribution from symbionts which is caused by dark conditions. This explains the differences in the ecological requirements of the two species. Because cyanobacterial symbionts release fixed carbon in the form of glycerol and other small organic phosphate (Wilkinson 1979), a model based on the glycerol 3-phosphate shuttle (typically occurring in chloroplasts and mitochondria) is suggested. The mechanism proposed appears to be an ancient biochemical adaptation which arose among ancestral symbiotic systems, and further developed in the relationships between endosymbiotic organelles and cytoplasm.