Molecular/chemical ecology in sponges: evidence for an adaptive antibacterial response in Suberites domuncula

Sponges (Porifera) represent the evolutionary oldest metazoan phylum still extant today. They have developed a complex Bauplan, based on the existence of structural and regulatory molecules; many of these have been cloned and analyzed in the past years. The demosponge Suberites domuncula has been used as a suitable model to demonstrate that these animals not only possess an adaptive immune response on the level of cytokines, but also, as pointed out here, on the level of synthesis of bioactive alkyl-lipid derivatives. From specimens of S. domuncula the two lyso-PAF (platelet-activating factor) compounds, 1-O-hexadecyl-sn-glycero-3-phosphocholine and 1-O-octadecyl-sn-glycero-3-phosphocholine, have been identified and characterized. These two lyso-PAFs showed pronounced anti-bacterial activity. In the central part of this paper it is shown that the level of synthesis of the lyso-PAF congeners increased in response to the model compound, the endotoxin lipopolysaccharide (LPS). Treatment of the tissue with LPS for 72 h substantially increased the synthesis. In order to prove that the lyso-PAFs are really synthesized by the sponge, the key enzyme of the alkyl-dihydroxyacetonephosphate pathway, i.e. alkyl-dihydroxyacetonephosphate synthase (ADS), was cloned from S. domuncula. This sponge enzyme comprises the characteristic features of metazoan ADS enzymes; it is increasingly expressed in the tissue and in the in vitro cell culture system after exposure to LPS. These data are taken as a strong indication that bioactive, low-molecular weight, non-proteinaceous lipid derivatives function in an adaptive manner in response to the endotoxin.