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Mechanisms involved in pearlfish resistance to holothuroid toxins

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Abstract

Holothuroids produce triterpenoid saponins that act as chemical defenses against predators and parasites. These saponins interact with sterols of the plasma membranes, inducing the formation of pores and then cell lysis. To avoid such harms from their own saponins, holothuroids present specific sterols in their tissues. Despite the noxious cytotoxic effect of their chemical defenses, holothuroids host various associates that display specific adaptations to resist to saponin toxicity. Among them, symbiotic carapid fishes (i.e., pearlfishes) are resistant to ichthyotoxic saponins as they display no stress response and a survival time 45 times longer than free-living fishes without any specific gill adaptation. The present study aims at discovering the resistance mechanism(s) developed by carapids by addressing 3 hypotheses: carapids have (1) a mechanical barrier against the toxin constituted by a larger secretion of mucus than other fishes, (2) a bioactive barrier against the toxins constituted by a mucus effective on saponins and (3) a Δ7sterol tissue composition mimicking holothuroids that enable them to resist to saponins. First experiments showed that the mucus has no effective impact on saponin chemical structures. Mass spectrometry analyses showed that carapids, similarly to non-symbiotic fishes but contrary to their hosts, present a Δ5sterol tissue composition. However, two different procedures have shown that carapids produce six to ten times more mucus than control fishes, suggesting that a great quantity of mucus can protect carapids from their host’s saponins and acts as a mechanical barrier against toxins. Therefore, these results provide a new understanding of the carapids–holothuroids relationship.

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Acknowledgments

The authors thank the IH.SM (Toliara, Madagascar) for having allowed them to carry out their experiments within their institute and M. Todesco for technical assistance. This work was supported by a FRFC project (FNRS, Fonds National de la Recherche Scientifique). This study is a contribution by the Centre Interuniversitaire de Biologie Marine (CIBIM). The UMONS MS Lab is grateful to the FNRS for financial support in the acquisition of the Waters QToF Premier Mass Spectrometer and for continuing support. GC benefited and thanks the fund Leopold III and the grant Agathon de Potter.

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Authors and Affiliations

  1. Biology of Marine Organisms and Biomimetics Unit, Research Institute for Biosciences, University of Mons (UMONS), 23, Place du Parc, 7000, Mons, Belgium

    Lola Brasseur, Guillaume Caulier, Patrick Flammang & Igor Eeckhaut

  2. Laboratory of Morphology, University of Liège (ULG), B6 Sart Tilman, 4000, Liège, Belgium

    Eric Parmentier

  3. Laboratory of Zoology, Research Institute for Biosciences, University of Mons (UMONS), 23, Place du Parc, 7000, Mons, Belgium

    Maryse Vanderplanck & Denis Michez

  4. Organic Synthesis and Mass Spectrometry Laboratory, Research Institute for Biosciences, University of Mons (UMONS), 23, Place du Parc, 7000, Mons, Belgium

    Pascal Gerbaux

  5. Unit of Analytical Chemistry, Gembloux Agro-Bio Tech-ULG, 2, Passage des Déportés, 5030, Gembloux, Belgium

    Georges Lognay

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  1. Lola Brasseur
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Correspondence to Lola Brasseur.

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Brasseur, L., Parmentier, E., Caulier, G. et al. Mechanisms involved in pearlfish resistance to holothuroid toxins. Mar Biol 163, 129 (2016). https://doi.org/10.1007/s00227-016-2901-3

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