Abstract
Background One of the most charismatic, and yet mostly unexplained example of mutualistic interaction is the partnership of clownfish and its symbiotic sea anemone. The mechanism explaining this tolerance currently relies on the molecular mimicry of clownfish epithelial mucus, which could serve as camouflage, preventing the anemone's nematocysts' discharge. Resident bacteria are known as key drivers of epithelial mucus chemical signature in vertebrates. A recent study has proposed a restructuration of the skin microbiota in a generalist clown fish when first contacting its symbiotic anemone. We explored a novel hypothesis by testing the effect of remote interaction on epithelial microbiota restructuration in both partners. Methods With metataxonomics, we investigated epithelial microbiota dynamics of 18 pairs of percula clownfish (Amphiprion percula) and their symbiotic anemone Heteractis magnifica in remote interaction, physical interaction and control groups for both partners during a four weeks trial.Results Physical and Remote Interaction groups’ results evidence epithelial microbiota convergence between both partners as soon as 15 minutes after fish and anemone have been placed in the same water system. This convergence occurred preceding any physical contact between partners, and was maintained during the two-weeks interaction period in both contact groups. After the interaction period, community structure of test anemones gradually shifted back to the state of their controls, whereas skin community structure of test clownfish maintained the interaction signature two weeks after fish-anemone pairs separation. Furthermore, the interaction signature persistence was observed both in Physical and Remote Interaction group fishes, thus suggesting that water-mediated chemical communication between symbiotic partners was strong enough to shift the skin microbiota durably, even after fish-anemone pairs separation. Finally, our results suggest that fish-anemone convergent microbiota restructuration was increasingly associated with the parallel recruitment of three Flavobacteriaceae strains closely related to a tyrosinase-producing Cellulophaga tyrosinoxydans. Conclusions Our study shows that bacterial community restructuration, in the acclimation process, does not only rely on direct physical contact. Furthermore, our results challenge, for the first time, the traditional unidirectional chemical camouflage hypothesis, as we argue that convergence of the epithelial microbiota of both partners may play essential roles in establishing mutual acceptance.