Lipopeptides from Cyanobacteria : structure and role in a trophic cascade

Abstract : In the lagoon of Moorea in French Polynesia, we have identified a relatively simple tropical marine ecosystem consisting of two primary producers (two filamentous cyanobacteria, Lyngbya majuscula and Anabaena cf. torulosa), three herbivorous molluscs (Stylocheilus striatus, S. longicauda and Bulla orientalis), a carnivorous nudibranch (Gymnodoris ceylonica) and a carnivorous crab (Thalamita coerulipes). L. majuscula and A. cf torulosa, that bloom ephemerally across wide sandy areas and even on corals, are prolific producers of secondary metabolites, mainly cyclic lipopeptides, which may either be toxic or act as feeding deterrents to potential consumers. However, these compounds do not prevent the sea hare S. striatus, feeding on cyanobacteria. S. striatus, considered as L. majuscula specialist, is known to sequester and transform some secondary metabolites produced by L. majuscula,. However we found also S. striatus feeding on A. cf torulosa and in this case it was less susceptible to predation by the nudibranch G. ceylonicasa than when it fed on L. majuscula. In the study of this model ecosystem, we combine cyanobacterial metabolome profiling and ecological bioassays in order to study the cascading effects of chemical mediators in multi-trophic relationships; we completed the metabolic profile characterization of the two cyanobacteria, we studied vertical and horizontal transmissions of the cyanobacterial secondary metabolites along the trophic web, and studied the role of these compounds in predator-prey relationships. Focusing our attention on A. cf torulosa we isolated seven new lipopeptides, derived from the known laxaphycins, and characterized them using extensive NMR experiments (1D and 2D NMR: COSY, TOCSY, HSQC, HMBC, NOESY), mass spectrometry (HR-MS and fragmentation by MSn) and Marfey’s advanced method. It is the first time that acyclic analogs of laxaphycins have been described. Although the peptides from L. majuscula are found intact in herbivores, some lipopeptides from A. cf torulosa are biotransformed by sea hares into four new compounds we characterized. The sequestration and biotransformation by the herbivores may be considered as a tolerance mechanism rather than a defense mechanism. We demonstrate also that the herbivores use cyanobacterial compounds as chemical cues for cyanobacteria tracking and feeding choice. Our experiments suggest that S. striatus and B. orientalis are generalist consumers, although the influence of cyanobacterial chemical cues on their foraging preferences may suggest an adaptive behavior enabling the mollusc to track their host of origin.
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Louis Bornancin. Lipopeptides from Cyanobacteria : structure and role in a trophic cascade. Other. Université Montpellier, 2016. English. ⟨NNT : 2016MONTT202⟩. ⟨tel-02478948⟩

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