When a repellent becomes an attractant: harmful saponins are kairomones attracting the symbiotic Harlequin crab

Abstract

Marine organisms have developed a high diversity of chemical defences in order to avoid predators and parasites. In sea cucumbers, saponins function as repellents and many species produce these cytotoxic secondary metabolites. Nonetheless, they are colonized by numerous symbiotic organisms amongst which the Harlequin crab, Lissocarcinus orbicularis, is one of the most familiar in the Indo-Pacific Ocean. We here identify for the first time the nature of the molecules secreted by sea cucumbers and attracting the symbionts: saponins are the kairomones recognized by the crabs and insuring the symbiosis. The success of this symbiosis would be due to the ability that crabs showed during evolution to bypass the sea cucumber chemical defences, their repellents becoming powerful attractants. This study therefore highlights the complexity of chemical communication in the marine environment.C hemical sensing is considered as the most ancient and the most ubiquitous mode of communication in the biosphere 1 ; all living organisms are able to detect chemical cues in their environments 2,3 . These cues allow different types of intra-and interspecific interactions between organisms, including, for example, mate recognition, prey-predator interactions and symbiotic associations. Indeed, communication between symbionts and their hosts is needed to insure appropriate host selection and the maintenance of the symbiotic relationship through time. Chemical signals emitted by hosts are named kairomones when they elicit a commensal or a parasitic symbiosis and synomones for mutualistic ones. Symbiotic associations are very common in echinoderms 4 and it is well known that echinoderms scent can attract various symbionts. This has been highlighted through different behavioural experiments on symbiotic polychaetes 5-7 , bivalves 8 , fishes 9 , crabs 10 , brittle stars 11 and shrimps 12,13 . All these studies showed that odours emitted by echinoderms in surrounding seawater are detected by symbionts and trigger an attractive chemotaxy. However, the exact chemical nature of the olfactory signals involved in the selection of an echinoderm host has never been discovered. In fact, up to now, only one semiochemical involved in a marine symbiosis has been identified: the amphikuemin, a synomone secreted by some species of sea anemones and recognized by clown fishes 14 .On the other hand, echinoderms are also well known for possessing defensive chemicals 15,16 that deter predation or prevent organisms to establish on their body. These allomones, semiochemicals providing a benefit to their producers, have been described in many representatives from the five echinoderm classes, but the most studied are the noxious saponins produced by sea stars (asteroids) 17,18 and sea cucumbers (holothuroids) 19 . Saponins are secondary metabolites first discovered in higher plants 20 that are also present in several marine sponges 21 . In sea cucumbers, saponins are found in the body wall and in the viscera, including the adhesive Cuvieran tubules. Structurally,...

Discovery of Novel Saponins from the Viscera of the Sea Cucumber Holothuria lessoni

“…lessoni . They reported saponins with m/z values of 1141, 1229, 1243 and 1463 namely Desholothurin A, Holothurin A 2 , Scabraside B (synonymous with Holothurin A) and Holothurinoside H, respectively [58]. However, we could not detect the ion at m/z 1463 in our sample.…”

Chemicals released by male sea cucumber mediate aggregation and spawning behaviours

“…Saponins are among the most important and abundant secondary metabolites of sea cucumbers, and have been reported to be involved in the chemical communication of marine organisms 75 , 76 . Although we cannot exclude the involvement of saponins in the spawning process, none of the detected compounds show mass spectral properties consistent with the reported for sea cucumber saponins.…”

Structural Elucidation of Novel Saponins in the Sea Cucumber Holothuria lessoni

“…Sea cucumbers expel their internal organs as a defense mechanism called evisceration, a reaction that includes release of the respiratory tree, intestine, cuvierian tubules and gonads through the anal opening [59,67,68,69,70,71,72,73,74]. The deterrent effect of saponins seems, therefore, to act as an aposematic signal, warning potential predators of the unpalatability of the holothuroid tissues [70].…”

“…The deterrent effect of saponins seems, therefore, to act as an aposematic signal, warning potential predators of the unpalatability of the holothuroid tissues [70]. In contrast, a recent study has shown that these repellent chemicals are also kairomones attracting the symbionts and are used as chemical “communicates” [67]. However, in the sea cucumber, it was suggested that saponins may also have two regulatory roles during reproduction: (1) to prevent oocyte maturation and (2) to act as a mediator of gametogenesis [25,75].…”