Mechanisms involved in pearlfish resistance to holothuroid toxins

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.