Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites

Abstract

Abstract Background Animal-associated microbial communities appear to be key factors in host physiology, ecology, evolution and its interactions with the surrounding environment. Teleost fish have received relatively little attention in the study of surface-associated microbiota. Besides the important role of microbiota in homeostasis and infection prevention, a few recent studies have shown that fish mucus microbiota may interact with and attract some specific parasitic species. However, our understanding of external microbial assemblages, in particular regarding the factors that determine their composition and potential interactions with parasites, is still limited. This is the objective of the present study that focuses on a well-known fish-parasite interaction, involving the Sparidae (Teleostei), and their specific monogenean ectoparasites of the Lamellodiscus genus. We characterized the skin and gill mucus bacterial communities using a 16S rRNA amplicon sequencing, tested how fish ecological traits and host evolutionary history are related to external microbiota, and assessed if some microbial taxa are related to some Lamellodiscus species. Results Our results revealed significant differences between skin and gill microbiota in terms of diversity and structure, and that sparids establish and maintain tissue and species-specific bacterial communities despite continuous exposure to water. No phylosymbiosis pattern was detected for either gill or skin microbiota, suggesting that other host-related and environmental factors are a better regulator of host-microbiota interactions. Diversity and structure of external microbiota were explained by host traits: host species, diet and body part. Numerous correlations between the abundance of given bacterial genera and the abundance of given Lamellodiscus species have been found in gill mucus, including species-specific associations. We also found that the external microbiota of the only unparasitized sparid species in this study, Boops boops, harbored significantly more Fusobacteria and three genera, Shewenella, Cetobacterium and Vibrio, compared to the other sparid species, suggesting their potential involvement in preventing monogenean infection. Conclusions This study is the first to explore the diversity and structure of skin and gill microbiota from a wild fish family and present novel evidence on the links between gill microbiota and monogenean species in diversity and abundance, paving the way for further studies on understanding host-microbiota-parasite interactions.