Choose Your Weaponry: Selective Storage of a Single Toxic Compound, Latrunculin A, by Closely Related Nudibranch Molluscs

Cheney, Karen L.; White, Andrew M.; Mudianta, I Wayan; Winters, Anne E.; Quezada, Michelle; Capon, Robert J.; Mollo, Ernesto; Garson, Mary J.

doi:10.1371/journal.pone.0145134

Cited by 50 publications

(71 citation statements)

References 55 publications

(72 reference statements)

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“…However, as is true for plants that simultaneously use visual and olfactory aposematic signals for animal attraction (45), T. striata uses double signaling, but for defensive purposes, whereas M. edwardsi relies on olfactory aposematism, which may provide protection from a wider range of predators, including those lacking efficient visual systems (35). It is worth underlining here that compounds 1-3 induce both toxic and olfactory-guided food avoidance effects and, differently from the cases considered by Eisner and Grant (44), they function as conditioned olfactory stimuli for indicating their own intrinsic toxicity and unprofitability.…”

Section: Discussionmentioning

confidence: 99%

“…The feeding deterrence activity of compounds 1-3 was evaluated against the cooccurring generalist shrimp Palaemon elegans Rathke, 1837, following an approach already used to assess the palatability of other bioactive metabolites (31), including marine furanosesquiterpenes (32,33). Like other palaemonid species (34,35), P. elegans is suitable for evaluations of this kind, which require a good view of the ingested food in the digestive system (31). Given that decapod crustaceans exhibit complex learning ability (36,37), the possibility that the shrimp learn to avoid the compounds after experiencing aversive olfactory stimuli was also considered.…”

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confidence: 99%

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Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments

Giordano

Carbone

Ciavatta

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Olfaction is considered a distance sense; hence, aquatic olfaction is thought to be mediated only by molecules dissolved in water. Here, we challenge this view by showing that shrimp and fish can recognize the presence of hydrophobic olfactory cues by a "tactile" form of chemoreception. We found that odiferous furanosesquiterpenes protect both the Mediterranean octocoral Maasella edwardsi and its specialist predator, the nudibranch gastropod Tritonia striata, from potential predators. Food treated with the terpenes elicited avoidance responses in the cooccurring shrimp Palaemon elegans. Rejection was also induced in the shrimp by the memory recall of postingestive aversive effects (vomiting), evoked by repeatedly touching the food with chemosensory mouthparts. Consistent with their emetic properties once ingested, the compounds were highly toxic to brine shrimp. Further experiments on the zebrafish showed that this vertebrate aquatic model also avoids food treated with one of the terpenes, after having experienced gastrointestinal malaise. The fish refused the food after repeatedly touching it with their mouths. The compounds studied thus act simultaneously as (i) toxins, (ii) avoidance-learning inducers, and (iii) aposematic odorant cues. Although they produce a characteristic smell when exposed to air, the compounds are detected by direct contact with the emitter in aquatic environments and are perceived at high doses that are not compatible with their transport in water. The mouthparts of both the shrimp and the fish have thus been shown to act as "aquatic noses," supporting a substantial revision of the current definition of the chemical senses based upon spatial criteria. T raditionally, the sense of smell has been regarded as a distance sense (like vision), whereas the sense of taste has been treated as a contact sense (like touch). This classification of the chemical senses (olfaction and gustation) based on their spatial range persists in contemporary literature. Accordingly, biomolecules smaller than ∼300 Da, which can be transported through air, and which finally bind to odorant receptors expressed in olfactory neurons, are generally considered odorant molecules. Conversely, the molecules sensed by taste have to be in solution and in contact with the receptor (1). However, the claim that "only olfaction can provide information on the identity of the water mass encountered" by marine organisms (2) implies that water-soluble compounds, which are typically "tasted" by the tongues of terrestrial animals, act as olfactory cues in aquatic environments. Consequently, it may be asked how typical odorant molecules such as small terpenes from plants and marine sponges that combine high volatility in air with insolubility in water can produce olfactory sensations in marine organisms, thereby giving protection from predators and cues to finding food and mates.

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments

Giordano

Carbone

Ciavatta

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…Some closely-related Chromodoris spp. have been shown to selectively accumulate a 16-membered macrolide, latrunculin A, in the mantle parts, leaving other secondary metabolites in the viscera [30]. A recent study has reported the exclusive incorporation of (−)-furodysinin in the dorsal horn of Ceratosoma trilobatum and Ceratosoma gracilimum , emphasizing the protective function of the dorsal horn in Ceratosoma nudibranchs [31].…”

Section: Resultsmentioning

confidence: 99%

The Sequestration of Oxy-Polybrominated Diphenyl Ethers in the Nudibranchs Miamira magnifica and Miamira miamirana

et al. 2016

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A series of oxy-polybrominated diphenyl ethers (O-PBDEs) has been isolated from the extracts of Miamira magnifica and Miamira miamirana collected from Queensland, Australia. M. magnifica sequesters the new OH-PBDE 1 and six known OH-PBDEs containing four to six bromines (2–7). M. miamirana also accumulates known tribromo- and tetrabromo OMe-PBDEs 8–10 in both mantle and viscera tissues. To date, Miamira is the only genus of the family Chromodorididae that is known to incorporate O-PBDEs, rather than terpenes, in the mantle where the metabolites may play a putative role in chemical defense. The extract of M. magnifica was tested in a brine shrimp lethality assay and exhibited an LD50 of 58 μg/mL.

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“…However, they emphasize a lot of evidence showing that the actual producers of the bioactive substances are associated microorganisms (mainly heterotrophic bacteria and cyanobacteria). In addition, a trophic transfer of the compounds from sponges to their specialist nudibranch predators is also described …”

Section: Marine Natural Products As Sources Of New Anticancer Drugsmentioning

confidence: 99%

Marine Mollusk‐Derived Agents with Antiproliferative Activity as Promising Anticancer Agents to Overcome Chemotherapy Resistance

Ciavatta

Lefranc

Carbone

et al. 2016

Medicinal Research Reviews

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The chemical investigation of marine mollusks has led to the isolation of a wide variety of bioactive metabolites, which evolved in marine organisms as favorable adaptations to survive in different environments. Most of them are derived from food sources, but they can be also biosynthesized de novo by the mollusks themselves, or produced by symbionts. Consequently, the isolated compounds cannot be strictly considered as “chemotaxonomic markers” for the different molluscan species. However, the chemical investigation of this phylum has provided many compounds of interest as potential anticancer drugs that assume particular importance in the light of the growing literature on cancer biology and chemotherapy. The current review highlights the diversity of chemical structures, mechanisms of action, and, most importantly, the potential of mollusk‐derived metabolites as anticancer agents, including those biosynthesized by mollusks and those of dietary origin. After the discussion of dolastatins and kahalalides, compounds previously studied in clinical trials, the review covers potentially promising anticancer agents, which are grouped based on their structural type and include terpenes, steroids, peptides, polyketides and nitrogen‐containing compounds. The “promise” of a mollusk‐derived natural product as an anticancer agent is evaluated on the basis of its ability to target biological characteristics of cancer cells responsible for poor treatment outcomes. These characteristics include high antiproliferative potency against cancer cells in vitro, preferential inhibition of the proliferation of cancer cells over normal ones, mechanism of action via nonapoptotic signaling pathways, circumvention of multidrug resistance phenotype, and high activity in vivo, among others. The review also includes sections on the targeted delivery of mollusk‐derived anticancer agents and solutions to their procurement in quantity.

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Choose Your Weaponry: Selective Storage of a Single Toxic Compound, Latrunculin A, by Closely Related Nudibranch Molluscs

Cited by 50 publications

References 55 publications

Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments

Volatile secondary metabolites as aposematic olfactory signals and defensive weapons in aquatic environments

The Sequestration of Oxy-Polybrominated Diphenyl Ethers in the Nudibranchs Miamira magnifica and Miamira miamirana

Marine Mollusk‐Derived Agents with Antiproliferative Activity as Promising Anticancer Agents to Overcome Chemotherapy Resistance

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