Cargando…

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

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Scheifler, Mathilde, Sanchez-Brosseau, Sophie, Magnanou, Elodie, Desdevises, Yves
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9009028/
https://www.ncbi.nlm.nih.gov/pubmed/35418308
http://dx.doi.org/10.1186/s42523-022-00180-1
_version_ 1784687187008159744
author Scheifler, Mathilde
Sanchez-Brosseau, Sophie
Magnanou, Elodie
Desdevises, Yves
author_facet Scheifler, Mathilde
Sanchez-Brosseau, Sophie
Magnanou, Elodie
Desdevises, Yves
author_sort Scheifler, Mathilde
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00180-1.
format Online
Article
Text
id pubmed-9009028
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-90090282022-04-15 Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites Scheifler, Mathilde Sanchez-Brosseau, Sophie Magnanou, Elodie Desdevises, Yves Anim Microbiome Research Article 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s42523-022-00180-1. BioMed Central 2022-04-13 /pmc/articles/PMC9009028/ /pubmed/35418308 http://dx.doi.org/10.1186/s42523-022-00180-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Scheifler, Mathilde
Sanchez-Brosseau, Sophie
Magnanou, Elodie
Desdevises, Yves
Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites
title Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites
title_full Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites
title_fullStr Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites
title_full_unstemmed Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites
title_short Diversity and structure of sparids external microbiota (Teleostei) and its link with monogenean ectoparasites
title_sort diversity and structure of sparids external microbiota (teleostei) and its link with monogenean ectoparasites
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9009028/
https://www.ncbi.nlm.nih.gov/pubmed/35418308
http://dx.doi.org/10.1186/s42523-022-00180-1
work_keys_str_mv AT scheiflermathilde diversityandstructureofsparidsexternalmicrobiotateleosteianditslinkwithmonogeneanectoparasites
AT sanchezbrosseausophie diversityandstructureofsparidsexternalmicrobiotateleosteianditslinkwithmonogeneanectoparasites
AT magnanouelodie diversityandstructureofsparidsexternalmicrobiotateleosteianditslinkwithmonogeneanectoparasites
AT desdevisesyves diversityandstructureofsparidsexternalmicrobiotateleosteianditslinkwithmonogeneanectoparasites