Sponge symbioses between Xestospongia deweerdtae and Plakortis spp. are not motivated by shared chemical defense against predators

Abstract

The recently described epizoic sponge-sponge symbioses between Xestospongia deweerdtae and two species of Plakortis present an unusual series of sponge interactions. Sponges from the genus Plakortis are fierce allelopathic competitors, rich in cytotoxic secondary metabolites, and yet X. deweerdtae flourishes as an epizoic encrustation on Plakortis deweerdtaephila and Plakortis symbiotica. Our objective in this study was to evaluate the hypothesis that X. deweerdtae grows epizoic to these two species of Plakortis due to a shared chemical defense against predators. We collected free-living individuals of X. deweerdtae and symbiotic pairs from a wide geographical range to generate crude organic extracts and a series of polarity fractions from sponge extract. We tested the deterrency of these extracts against three common coral reef predators: the bluehead wrasse, Thalassoma bifasciatum, the Caribbean sharpnose puffer, Canthigaster rostrata, and the white spotwrist hermit crab, Pagurus criniticornis. While the chemical defenses of P. deweerdtaephila and P. symbiotica are more potent than those of X. deweerdtae, all of the sponge species we tested significantly deterred feeding in all three generalist predators. The free-living form of X. deweerdtae is mostly defended across the region, with a few exceptions. The associated form of X. deweerdtae is always defended, and both species of Plakortis are very strongly defended, with puffers refusing to consume extract-treated pellets until the extract was diluted to 1/256× concentration. Using diode-array high performance liquid chromatography (HPLC) coupled with high-resolution mass spectrometry (LC-MS/IT-TOF), we found two secondary metabolites from P. deweerdtaephila, probably the cyclic endoperoxides plakinic acid I and plakinic acid K, in low concentrations in the associated—but not the free-living—form of X. deweerdtae, suggesting a possible translocation of defensive chemicals from the basibiont to the epibiont. Comparing the immense deterrency of Plakortis spp. extracts to the extracts of X. deweerdtae gives the impression that there may be some sharing of chemical defenses: one partner in the symbiosis is clearly more defended than the other and a small amount of its defensive chemistry may translocate to the partner. However, X. deweerdtae effectively deters predators with its own defensive chemistry. Multiple lines of evidence provide no support for the shared chemical defense hypothesis. Given the diversity of other potential food resources available to predators on coral reefs, it is improbable that the evolution of these specialized sponge-sponge symbioses has been driven by predation pressure.

Marine natural products

“…Correlating the deterrent activity of associated and non-associated sponge specimens indicated that both members of the symbiosis benet from the presence of the other through shared metabolic defensive chemistry, although it is suggested that Plakortis is more chemically defended than Xestospongia and only minimal translocation of metabolites is likely. 519 The production of discodermolide in aquaculture studies of Discodermia dissoluta at two sites in the Colombian Caribbean using xed or suspended culturing showed that production of the target compound was independent of both location and the conditions used, although a negative correlation with temperature was noted. Production of this important bioactive compound ranged from 20-270 mg g À1 of dry sponge.…”

Probing the Antiplasmodial Properties of Plakortinic Acids C and D: An Uncommon Pair of Marine Peroxide-Polyketides Isolated from a Two-Sponge Association of Plakortis symbiotica and Xetospongia deweerdtae Collected near Puerto Rico

“…These compounds were isolated together as an inseparable mixture from the sy otic association of two Caribbean marine sponges, Plakortis symbiotica-Xestosp deweerdtae, collected on Mona Island, off the west coast of Puerto Rico [27]. This sponge consortium, originally classified as an association between Plakortis halichondr and Xetospongia deweerdtae [28,29], has been shown to host molecules with unique ch cal structures and exceptional bioactivities. For example, smenothiazole A, which played a MIC value of 4.1 µg/mL against Mycobacterium tuberculosis [30], along These compounds were isolated together as an inseparable mixture from the symbiotic association of two Caribbean marine sponges, Plakortis symbiotica-Xestospongia deweerdtae, collected on Mona Island, off the west coast of Puerto Rico [27].…”

Metabolites and Bioactivity of the Marine Xestospongia Sponges (Porifera, Demospongiae, Haplosclerida) of Southeast Asian Waters

“…Some Xestospongia spp. also form symbiotic relationships with other prokaryotes [ 23 , 29 , 30 , 31 ].…”