Abstract
BackgroundOne of the most charismatic, and yet not completely resolved 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.MethodsWith metataxonomics, we investigated the epithelial microbiota dynamic 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 4-week trial.ResultsThe Physical and Remote Interaction groups’ results evidence gradual epithelial microbiota convergence between both partners when fish and anemone were placed in the same water system. This convergence occurred preceding any physical contact between partners, and was maintained during the 2-week interaction period in both contact groups. After the interaction period, community structure of both fish and anemone’s epthelial community structures maintained the interaction signature 2 weeks after fish–anemone pairs’ separation. Furthermore, the interaction signature persistence was observed both in the Physical and Remote Interaction groups, thus suggesting that water-mediated chemical communication between symbiotic partners was strong enough to shift the skin microbiota durably, even after the separation of fish–anemone pairs. 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.ConclusionsOur 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.9p4RZDq8XFt4wx9Qb_GP5vVideo abstract Fish−anemone symbiotic relationship.
Highlights
One of the most charismatic, and yet not completely resolved example of mutualistic interaction is the partnership of clownfish and its symbiotic sea anemone
At T1, 15 min after the clownfish test individuals were transferred from the fish control tank system into their respective two-tank systems for remote interaction (RI), and after the first 15 min of physical contact between physical interaction (PI) clownfish individuals with their respective anemone, dissimilarity between test and control anemones was significantly higher relatively to that of T0
We provide salient insights supporting the multilayered model of microbiome structuring from Shapira [52], which proposes that the variable environmentally modulated flexible microbial pool, termed as transient microbiota, allows adaptation of holobionts to changing environments at the scale of microbial generation time
Summary
One of the most charismatic, and yet not completely resolved 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. Pratte et al [15] conducted an investigation targeting a generalist clownfish species (Amphiprion clarkii) known to have an innate mechanism of protection against nematocyst discharge Their experimental design included physical interaction groups that shared the same water flow than the fish control group [15], and the control group was constantly in remote interaction with fish–anemone pairs. We tested the hypothesis that there would be a gradual convergence of the skin mucus microbiota structure of both symbiotic partners during the interaction period, which would rely on physical contact
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