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.