Audet-Gilbert Émie1, Sylvain François-Étienne1, Bouslama Sidki1, Derome Nicolas2. 1. Institut de Biologie Intégrative et des Systèmes, Université Laval, 1030 avenue de la Médecine, Québec, QC, G1V 0A6, Canada. 2. Institut de Biologie Intégrative et des Systèmes, Université Laval, 1030 avenue de la Médecine, Québec, QC, G1V 0A6, Canada. nicolas.derome@bio.ulaval.ca.
Abstract
BACKGROUND: 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. 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 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. RESULTS: The 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. 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. Video abstract Fish-anemone symbiotic relationship.
BACKGROUND: 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. 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 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. RESULTS: The 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. 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. Video abstract Fish-anemone symbiotic relationship.
Authors: M S Llewellyn; S Leadbeater; C Garcia; F-E Sylvain; M Custodio; K P Ang; F Powell; G R Carvalho; S Creer; J Elliot; N Derome Journal: Sci Rep Date: 2017-03-07 Impact factor: 4.379
Authors: Christopher A Gaulke; Mauricio L Martins; Virginia G Watral; Ian R Humphreys; Sean T Spagnoli; Michael L Kent; Thomas J Sharpton Journal: Microbiome Date: 2019-01-24 Impact factor: 14.650