Anemonefish use sialic acid metabolism as Trojan horse to avoid giant sea anemone stinging

Abstract

Anemonefish association with giant sea anemone is an iconic example of mutualistic symbiosis. Living inside the sea anemone without triggering the firing of highly toxic nematocysts present at the surface of sea anemone tentacles provides a unique shelter to the fish, which in return, by its territorial aggressiveness, protects the sea anemone from predators. The mechanisms by which the fish avoids triggering nematocysts discharge remain elusive. One hypothesis proposes that absence of sialic acids might disable nematocysts discharge. Here, we verified four predictions about the role of sialic acids in anemonefish protection: (i) sialic acid levels are lower in anemonefish mucus than in non-symbiotic and sensitive damselfish mucus; (ii) this decrease is specific to mucus and not observed in other organs; (iii) during post-embryonic development the levels of sialic acids are inversely correlated with the level of protection; (iv) the levels of sialic acids are minimal in sea anemone mucus. Taken together, our results allow us to propose a general model, in which anemonefish specifically regulates the level of sialic acids in their mucus to avoid nematocysts discharge. Our analysis also highlights several genes implicated in sialic acid removal as potential targets for allowing protection. Interestingly, our results also suggest that unrelated juveniles of damselfish (Dascyllus trimaculatus) capable to live in proximity with giant sea anemone may use the same mechanisms. Altogether, our data suggest that clownfish use sialic acids as a Trojan horse system to downplay the defenses of the sea anemones and illustrate the convergent tinkering used by fish to allow a mutualistic association with their hosts. Significance statementThe mutualistic relationship between anemonefish and giant sea anemones, where the fish shelter among the anemones tentacles while defending it from predators, is a classic example of symbiosis. However, how the fish avoids triggering the anemones venomous nematocysts has remained a mystery. This study reveals that the fish decrease the levels of sialic acids in their mucus, potentially preventing nematocyst discharge. This finding shed light on the mechanisms underlying this symbiotic relationship. Moreover, the discovery that unrelated damselfish may employ similar strategies underscores the broader significance of convergent adaptations in facilitating similar mutualistic associations in marine fishes.