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Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore

BACKGROUND: Holobionts have a digestive microbiota with catabolic abilities allowing the degradation of complex dietary compounds for the host. In terrestrial herbivores, the digestive microbiota is known to degrade complex polysaccharides from land plants while in marine herbivores, the digestive m...

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Autores principales: Gobet, Angélique, Mest, Laëtitia, Perennou, Morgan, Dittami, Simon M, Caralp, Claire, Coulombet, Céline, Huchette, Sylvain, Roussel, Sabine, Michel, Gurvan, Leblanc, Catherine
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5870069/
https://www.ncbi.nlm.nih.gov/pubmed/29587830
http://dx.doi.org/10.1186/s40168-018-0430-7
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author Gobet, Angélique
Mest, Laëtitia
Perennou, Morgan
Dittami, Simon M
Caralp, Claire
Coulombet, Céline
Huchette, Sylvain
Roussel, Sabine
Michel, Gurvan
Leblanc, Catherine
author_facet Gobet, Angélique
Mest, Laëtitia
Perennou, Morgan
Dittami, Simon M
Caralp, Claire
Coulombet, Céline
Huchette, Sylvain
Roussel, Sabine
Michel, Gurvan
Leblanc, Catherine
author_sort Gobet, Angélique
collection PubMed
description BACKGROUND: Holobionts have a digestive microbiota with catabolic abilities allowing the degradation of complex dietary compounds for the host. In terrestrial herbivores, the digestive microbiota is known to degrade complex polysaccharides from land plants while in marine herbivores, the digestive microbiota is poorly characterized. Most of the latter are generalists and consume red, green, and brown macroalgae, three distinct lineages characterized by a specific composition in complex polysaccharides, which represent half of their biomass. Subsequently, each macroalga features a specific epiphytic microbiota, and the digestive microbiota of marine herbivores is expected to vary with a monospecific algal diet. We investigated the effect of four monospecific diets (Palmaria palmata, Ulva lactuca, Saccharina latissima, Laminaria digitata) on the composition and specificity of the digestive microbiota of a generalist marine herbivore, the abalone, farmed in a temperate coastal area over a year. The microbiota from the abalone digestive gland was sampled every 2 months and explored using metabarcoding. RESULTS: Diversity and multivariate analyses showed that patterns of the microbiota were significantly linked to seasonal variations of contextual parameters but not directly to a specific algal diet. Three core genera: Psychrilyobacter, Mycoplasma, and Vibrio constantly dominated the microbiota in the abalone digestive gland. Additionally, a less abundant and diet-specific core microbiota featured genera representing aerobic primary degraders of algal polysaccharides. CONCLUSIONS: This study highlights the establishment of a persistent core microbiota in the digestive gland of the abalone since its juvenile state and the presence of a less abundant and diet-specific core community. While composed of different microbial taxa compared to terrestrial herbivores, the digestive gland constitutes a particular niche in the abalone holobiont, where bacteria (i) may cooperate to degrade algal polysaccharides to products assimilable by the host or (ii) may have acquired these functions through gene transfer from the aerobic algal microbiota. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0430-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-58700692018-03-29 Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore Gobet, Angélique Mest, Laëtitia Perennou, Morgan Dittami, Simon M Caralp, Claire Coulombet, Céline Huchette, Sylvain Roussel, Sabine Michel, Gurvan Leblanc, Catherine Microbiome Research BACKGROUND: Holobionts have a digestive microbiota with catabolic abilities allowing the degradation of complex dietary compounds for the host. In terrestrial herbivores, the digestive microbiota is known to degrade complex polysaccharides from land plants while in marine herbivores, the digestive microbiota is poorly characterized. Most of the latter are generalists and consume red, green, and brown macroalgae, three distinct lineages characterized by a specific composition in complex polysaccharides, which represent half of their biomass. Subsequently, each macroalga features a specific epiphytic microbiota, and the digestive microbiota of marine herbivores is expected to vary with a monospecific algal diet. We investigated the effect of four monospecific diets (Palmaria palmata, Ulva lactuca, Saccharina latissima, Laminaria digitata) on the composition and specificity of the digestive microbiota of a generalist marine herbivore, the abalone, farmed in a temperate coastal area over a year. The microbiota from the abalone digestive gland was sampled every 2 months and explored using metabarcoding. RESULTS: Diversity and multivariate analyses showed that patterns of the microbiota were significantly linked to seasonal variations of contextual parameters but not directly to a specific algal diet. Three core genera: Psychrilyobacter, Mycoplasma, and Vibrio constantly dominated the microbiota in the abalone digestive gland. Additionally, a less abundant and diet-specific core microbiota featured genera representing aerobic primary degraders of algal polysaccharides. CONCLUSIONS: This study highlights the establishment of a persistent core microbiota in the digestive gland of the abalone since its juvenile state and the presence of a less abundant and diet-specific core community. While composed of different microbial taxa compared to terrestrial herbivores, the digestive gland constitutes a particular niche in the abalone holobiont, where bacteria (i) may cooperate to degrade algal polysaccharides to products assimilable by the host or (ii) may have acquired these functions through gene transfer from the aerobic algal microbiota. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-018-0430-7) contains supplementary material, which is available to authorized users. BioMed Central 2018-03-27 /pmc/articles/PMC5870069/ /pubmed/29587830 http://dx.doi.org/10.1186/s40168-018-0430-7 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Gobet, Angélique
Mest, Laëtitia
Perennou, Morgan
Dittami, Simon M
Caralp, Claire
Coulombet, Céline
Huchette, Sylvain
Roussel, Sabine
Michel, Gurvan
Leblanc, Catherine
Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore
title Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore
title_full Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore
title_fullStr Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore
title_full_unstemmed Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore
title_short Seasonal and algal diet-driven patterns of the digestive microbiota of the European abalone Haliotis tuberculata, a generalist marine herbivore
title_sort seasonal and algal diet-driven patterns of the digestive microbiota of the european abalone haliotis tuberculata, a generalist marine herbivore
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5870069/
https://www.ncbi.nlm.nih.gov/pubmed/29587830
http://dx.doi.org/10.1186/s40168-018-0430-7
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