Abstract
Natural products play an invaluable role as a starting point in the drug discovery process, and plants and animals use many interesting biologically active natural products as a chemical defense mechanism against predators. Among marine organisms, many nudibranch gastropods are known to derive defensive metabolites from the sponges they eat. Here we investigated the putative sequestration of the toxic compound latrunculin A—a 16-membered macrolide that prevents actin polymerization within cellular processes—which has been identified from sponge sources, by five closely related nudibranch molluscs of the genus Chromodoris. Only latrunculin A was present in the rim of the mantle of these species, where storage reservoirs containing secondary metabolites are located, whilst a variety of secondary metabolites were found in their viscera. The species studied thus selectively accumulate latrunculin A in the part of the mantle that is more exposed to potential predators. This study also demonstrates that latrunculin-containing sponges are not their sole food source. Latrunculin A was found to be several times more potent than other compounds present in these species of nudibranchs when tested by in vitro and in vivo toxicity assays. Anti-feedant assays also indicated that latrunculin A was unpalatable to rock pool shrimps, in a dose-dependent manner. These findings led us to propose that this group of nudibranchs has evolved means both to protect themselves from the toxicity of latrunculin A, and to accumulate this compound in the mantle rim for defensive purposes. The precise mechanism by which the nudibranchs sequester such a potent compound from sponges without disrupting their own key physiological processes is unclear, but this work paves the way for future studies in this direction. Finally, the possible occurrence of both visual and chemosensory Müllerian mimicry in the studied species is discussed.
Highlights
Many natural products used in drug discovery are molecules that are used to protect plants and animals from consumers, and investigations into their chemical structure and bioactivity are numerous [1, 2]
Latrunculin A, a 16-membered macrolide with an attached 2-thiazolidinone unit, which was originally isolated from the Red Sea sponge Negombata magnifica (= Latrunculia magnifica) [6], and other Pacific sponges: Cacospongia mycofijiensis (= Spongia mycofijiensis, = Petrosaspongia mycofijiensis [7,8,9]), and Hyattela sp. [10], has been found in a group of sponge-feeding nudibranchs from the family Chromodorididae, including: Chromodoris elisabethina [11], Chromodoris lochi [7, 10], C. hamiltoni [12], and C. quadricolor [13]
We investigated the anatomical distribution of latrunculin A in a range of closely-related [33] nudibranch species: Chromodoris elisabethina, C. lochi, C. kuiteri, C. annae, C. magnifica
Summary
Many natural products used in drug discovery are molecules that are used to protect plants and animals from consumers, and investigations into their chemical structure and bioactivity are numerous [1, 2]. Bioactive compounds occur in many species of nudibranch mollusc (Mollusca: Gastropoda: Nudibranchia). Among these compounds, latrunculin A, a 16-membered macrolide with an attached 2-thiazolidinone unit, which was originally isolated from the Red Sea sponge Negombata magnifica (= Latrunculia magnifica) [6], and other Pacific sponges: Cacospongia mycofijiensis (= Spongia mycofijiensis, = Petrosaspongia mycofijiensis [7,8,9]), and Hyattela sp. Latrunculin A, a 16-membered macrolide with an attached 2-thiazolidinone unit, which was originally isolated from the Red Sea sponge Negombata magnifica (= Latrunculia magnifica) [6], and other Pacific sponges: Cacospongia mycofijiensis (= Spongia mycofijiensis, = Petrosaspongia mycofijiensis [7,8,9]), and Hyattela sp. Little is known about the distribution of both latrunculin A and the other mentioned compounds in the different body parts of the nudibranchs
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