Okadaic Acid, an Apoptogenic Toxin for Symbiotic/Parasitic Annelids in the Demosponge Suberites domuncula

Abstract

The role of okadaic acid (OA) in the defense system of the marine demosponge Suberites domuncula against symbiotic/parasitic annelids was examined. Bacteria within the mesohyl produced okadaic acid at concentrations between 32 ng/g and 58 ng/g of tissue (wet weight). By immunocytochemical methods and by use of antibodies against OA, we showed that the toxin was intracellularly stored in vesicles. Western blotting experiments demonstrated that OA also existed bound to a protein with a molecular weight of 35,000 which was tentatively identified as a galectin (by application of antigalectin antibodies). Annelids that are found in S. domuncula undergo apoptotic cell death. OA is one candidate inducer molecule of this process, since this toxin accumulated in these symbionts/parasites. Furthermore, we identified the cDNA encoding the multifunctional prosurvival molecule BAG-1 in S. domuncula; it undergoes strong expression in the presence of the annelid. Our data suggest that sponges use toxins (here, OA) produced from bacteria to eliminate metazoan symbionts/ parasites by apoptosis.Sponges, the evolutionarily oldest metazoan phylum (Porifera), share one common ancestor with the other metazoan phylum, the Urmetazoa (31, 35). Most sponges are marine sessile filter feeders; some species daily filter tons of water containing millions of bacteria or viruses through their bodies (48; reviewed in references 18 and 26). Due to their efficient chemical and biological defense systems, sponges have survived not only adverse climatic periods (24) but also biotic and anthropogenic threats (34).Two strategies are used by sponges to eliminate attacking (infectious) bacteria: first, chemical strategies via the production of secondary metabolites (see references 45 and 51) and, second, humoral and cellular defense mechanisms (33). The hitherto studied molecular biological or cell biological defense systems used by sponges against microorganisms have been elucidated primarily in the demosponge Suberites domuncula. This species is able to recognize and defeat gram-positive as well as gram-negative bacteria by the antimicrobial lectin tachylectin (52). In addition, S. domuncula has developed a specific system to recognize gram-positive bacteria via the peptidoglycan coat; subsequently bacteria are endocytosed and/or extracellularly digested by lysozyme (59). The lipopolysaccharide (LPS) outer membrane of gram-negative bacteria induces in S. domuncula an adaptive antibacterial response by increasing the release of bioactive and antimicrobial lyso-plateletactivating factors (36). We have shown that in the aqueous environment also, fungi are recognized by sponges via a receptor, the (133)-␤-D-glucan binding protein; after interaction of fungal (133)-␤-D-glucans with the corresponding receptor, S. domuncula causes the expression of a series of defense molecules, e.g., a fibrinogen-like protein and an epidermal growth factor precursor (43).Finally, the more general defense system against microorganisms should be highlighted; LPS activates th...

Okadaic Acid Meet and Greet: An Insight into Detection Methods, Response Strategies and Genotoxic Effects in Marine Invertebrates

“…This is indeed the case of the marine sponge Suberites domuncula harboring bacteria containing OA. Here, low OA concentrations (<100 nM) stimulate the defense system against bacteria [65], whereas high OA concentrations (>500 nM) induce apoptosis in symbiotic or parasitic annelids [65,66] while preventing self-intoxication in the sponge [67,68]. Furthermore, another type of defensive role for OA has been reported in the sponge Lubomirskia baicalensis , where OA seems to facilitate the expression of the heat shock protein hsp70 during the winter season, helping this species withstand water temperatures of 0 °C below the sea ice [69].…”

Chemical Defenses: From Compounds to Communities

“…No reports have identified the biosynthetic pathway of any secondary metabolite of dinoflagellate origin at the genomic level (Snyder et al, 2005). Although immunological evidence suggests that bacteria inside the sponge Suberites dumuncula as well as sponge cells and intracellular vacuoles all contain OA (Wiens et al, 2003;Schröder et al, 2006), no bacteria that produce a polyketide toxin have been isolated from a dinoflagellate (Wiens et al, 2003;Snyder et al, 2005).…”

“…At elevated concentrations (Ͼ500 nmol l -1 ), OA acts as an apoptogen and promotes expression of the proapoptotic caspase gene with a simultaneous down-regulation of the expression of the anti-apoptotic Bcl-2 homolog gene. In subsequent studies of S. domuncula, Schröder et al (2006) suggested that OA may serve as a defense molecule by inducing apoptosis in symbiotic or parasitic annelids. In other work, Müller et al (2007) demonstrated that OA is required for the expression of the heat shock protein hsp70 at low temperature and contributes to cold tolerance in the sponge Lubomirskia baicalensis.…”

Localization of ‘Candidatus Endobugula sertula’ and the bryostatins throughout the life cycle of the bryozoan Bugula neritina

“…Although several studies have successfully used visualization techniques to localize natural products in situ in various marine invertebrates (Gillor et al, 2000;Salomon et al, 2001;Schroder et al, 2006), the methods used in those studies are not feasible for use in bryostatin localization. In order to detect bryostatins in situ, we developed a method based on their clinical molecular target, mammalian protein kinase C (PKC).…”