Insights into the Natural Defenses of a Coral Reef Fish Against Gill Ectoparasites: Integrated Metabolome and Microbiome Approach.

Miriam Reverter,Nicolas Inguimbert,Alan Pare,Pierre Sasal,Delphine Raviglione,Marcelino T Suzuki,Philippe Bulet,Nathalie Tapissier-Bontemps,Sébastien N Voisin,Bernard Banaigs

doi:10.3390/metabo10060227

Abstract

Understanding natural defense mechanisms against parasites can be a valuable tool for the development of innovative therapies. We have previously identified a butterflyfish species (Chaetodon lunulatus) that avoids gill monogenean parasites while living amongst closely related parasitized species. The metabolome and microbiome of several sympatric butterflyfish species from the island of Moorea (French Polynesia) were previously described. In this study, we used the previously generated datasets in an attempt to identify metabolites and bacteria potentially involved in parasite defense mechanisms. We investigated the interplay between the gill mucus metabolome and microbiome of the non-susceptible C. lunulatus versus sympatric butterflyfish species that were always found parasitized in the Central and Eastern Indo-Pacific. After observing significant differences between the metabolome and bacteria of susceptible versus non-susceptible fish, we obtained the discriminant metabolites and operational taxonomic units (OTUs) using a supervised analysis. Some of the most important discriminant metabolites were identified as peptides, and three new peptides derived from β-subunit hemoglobin from C. lunulatus (CLHbβ-1, CLHbβ-2, and CLHbβ-3) were purified, characterized and synthesized to confirm their structures. We also identified specific bacterial families and OTUs typical from low-oxygen habitats in C. lunulatus gill mucus. By using a correlation network between the two datasets, we found a Fusobacteriaceae strain exclusively present in C. lunulatus and highly correlated to the peptides. Finally, we discuss the possible involvement of these peptides and Fusobacteriaceae in monogenean avoidance by this fish species.

Highlights

Parasites are crucial for a well-balanced ecosystem, contributing to its organization by modifying competitive and trophic interactions and driving natural selection [1]
We found that only one butterflyfish species (Chaetodon lunulatus) out of 34 species studied through the Indo-Pacific, was never parasitized by gill monogeneans [34]
We did not perform further identification, and correlation with bacterial operational taxonomic units (OTUs) were based on the analysis of the polar fraction

Summary

Introduction

Parasites are crucial for a well-balanced ecosystem, contributing to its organization by modifying competitive and trophic interactions and driving natural selection [1]. Understanding the factors underpinning host-parasite interactions is critical to prevent the emergence of infectious diseases that can result in biodiversity decrease and severe economic losses [5,6]. In this context, a better understanding of natural defense mechanisms can contribute to the development of alternative sustainable therapies both in human and animal medicine [7,8]. Despite the poor understanding of the role of native host microbiota against eukaryotic parasites is poorly understood, some studies suggest they can deploy multiple strategies to control parasitic infections. Cirimotich et al found that an Enterobacter bacterium from mosquito inhibited the development of malaria parasites by the production of reactive oxygen species (ROS), rendering mosquitoes resistant to infection [11]

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