Spherulization as a process for the exudation of chemical cues by the encrusting sponge C. crambe

Abstract

Ecological interactions in the marine environment are now recognized to be partly held by chemical cues produced by marine organisms. In particular, sponges are sessile animals thought to rely on the bioactive substances they synthesize to ensure their development and defense. However, the mechanisms leading the sponges to use their specialized metabolites as chemical cues remain unknown. Here we report the constant release of bioactive polycyclic guanidinic alkaloids by the Mediterranean sponge Crambe crambe into the dissolved and the particulate phases using a targeted metabolomics study. These compounds were proven to be stored into already described specialized (spherulous) sponge cells and dispersed into the water column after release through the sponge exhaling channels (oscula), leading to a chemical shield surrounding the sponge. Low concentrations of these compounds were demonstrated to have teratogenic effects on embryos of a common sea squirt (ascidian). This mechanism of action called spherulization may therefore contribute to the ecological success of encrusting sponges that need to extend their substrate cover to expand.

The culturable mycobiota associated with the Mediterranean sponges Aplysina cavernicola, Crambe crambe and Phorbas tenacior

“…Indeed, the toxic compounds produced by this sponge could strongly select the fungal community able to grow on the sponge and/or inhibit the fungal growth in the isolation plates. From an ecological point of view, these compounds, once released, have teratogen effects on ascidian embryos, supporting the hypothesis that encrusting sponges like C. crambe, use toxic metabolites to mediate the colonization of new habitats (Ternon et al 2016).…”

“…Actually, this sponge is well known for the production of toxic compounds (including polycyclic guanidine alkaloids), which are concentrated in the outer layer (Uriz et al 1996;Ternon et al 2016), making this organism scarcely colonisable by bacteria (Becerro et al 1997). In fact, C. crambe belongs to the -lowmicrobial-abundance sponges‖ characterized by an average amount of bacteria per g of sponge-wet weight lower than that of seawater (Sipkema et al 2015).…”

“…C. crambe has been widely studied since the early 1990s, for example, Uriz et al (1996) pointed out that the outer layer of this animal was more toxic than the inner one. This toxicity is probably due to polycyclic guanidine alkaloids, whose anticancer activity has been demonstrated (Ternon et al 2016). As for A. cavernicola, the production of secondary metabolites shows a seasonal fluctuation in this latter species (Becerro et al 1997).…”

Batzella, Crambe and Monanchora: Highly Prolific Marine Sponge Genera Yielding Compounds with Potential Applications for Cancer and Other Therapeutic Areas

“…Furthermore, crambescidin 816 ( 80 ) displayed potent Ca 2+ antagonist activity and inhibited the acetylcholine-induced contraction of guinea pig ileum within very low concentrations [ 17 ], however, recent novel evidence showed that compound 80 partially blocked CaV and NaV channels in neurons, proposes that this compound might be included in decreasing the neurotransmitter release and synaptic transmission within the central nervous system [ 76 ]. Further, recent study proved that crambescidin 816 ( 80 ) could be stored into specialized sponge cells where it can be dispersed into the water affording a chemical umbrella surrounding the Crambe crambe sponge [ 77 ]. Recently, Botana and co-workers [ 78 ] reported important insights about the mechanism of the neurons cytotoxic activity of crambescidin 816 ( 80 ) in primary cultures of cortical neurons.…”

Revealing the ocean metabolome with mass spectrometry

“…Exometabolomics provides an opportunity to directly characterize the molecular interaction between microbes and their environment by profiling the types of molecules cellular organisms secrete (5). In terrestrial and limnic systems, these studies have advanced our understanding of microbial communities in soil organic matter cycling (6, 7), overflow metabolism of cultivable microorganisms (8, 9) and chemical ecology of the environment (10, 11). While intracellular metabolomic analyses of tissues from marine microbial cells to invertebrates is becoming increasingly more common (12-14), the defining characteristic of marine habitats - high salt concentration - limits exometabolomic analyses of the oceans to studies that require salt removal prior to metabolite extraction (10, 15, 16).…”