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Dietary Exposure of Pacific Oyster (Crassostrea gigas) Larvae to Compromised Microalgae Results in Impaired Fitness and Microbiome Shift

The Pacific oyster Crassostrea gigas is the world’s most cultivated oyster and seed supply is heavily reliant on hatchery production where recurring mass mortality events are a major constraint. Outbreaks of bacterial infection via microalgal feed are frequently implicated in these mortalities. This...

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Autores principales: Vignier, Julien, Laroche, Olivier, Rolton, Anne, Wadsworth, Pandora, Kumanan, Karthiga, Trochel, Branwen, Pochon, Xavier, King, Nick
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8421776/
https://www.ncbi.nlm.nih.gov/pubmed/34504478
http://dx.doi.org/10.3389/fmicb.2021.706214
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author Vignier, Julien
Laroche, Olivier
Rolton, Anne
Wadsworth, Pandora
Kumanan, Karthiga
Trochel, Branwen
Pochon, Xavier
King, Nick
author_facet Vignier, Julien
Laroche, Olivier
Rolton, Anne
Wadsworth, Pandora
Kumanan, Karthiga
Trochel, Branwen
Pochon, Xavier
King, Nick
author_sort Vignier, Julien
collection PubMed
description The Pacific oyster Crassostrea gigas is the world’s most cultivated oyster and seed supply is heavily reliant on hatchery production where recurring mass mortality events are a major constraint. Outbreaks of bacterial infection via microalgal feed are frequently implicated in these mortalities. This study assessed the effects of feeding compromised microalgae to developing oyster larvae. Intentionally ‘stressed’ (high pH) or non-stressed microalgae were fed to 11 day-old oyster larvae at two feeding rations for 96 h, followed by a recovery period. Biological endpoints of larval performance were measured following the 96 h exposure and subsequent recovery. Bacterial communities associated with the microalgae feed, rearing seawater, and the oyster larvae, were characterized and correlated with effects on oyster fitness parameters. Feeding stressed algae to oyster larvae for 96 h increased the occurrence of deformities (>70% vs. 20% in control), reduced feeding and swimming ability, and slowed development. Following the recovery period, fewer larvae reached pediveliger stage (2.7% vs. 36% in control) and became spat (1.5% vs. 6.6% in control). The quantity of stressed algae supplied to oyster larvae also influenced overall larval performance, with high feeding rations generally causing greater impairment than low rations. Bacterial profiling using 16S rRNA showed that most bacterial families characterized in larval tissue were also present in larval rearing seawater and in the microalgae feed (98%). The rearing seawater showed the highest bacterial richness compared to the larval and the microalgal compartments, regardless of feeding regime. In larval tissue, bacterial richness was highest in stressed and high-feed treatments, and negatively correlated with larval fitness parameters. These results suggest significant dysbiosis induced by compromised feed and/or increased feed ration. Several bacterial genera (e.g., Halomonas, Marinomonas) were strongly associated with impaired larval performance while the presence of genera in larvae including Vibrio was closely associated with overfeeding. Our research demonstrated that metabarcoding can be effectively used to identify microbiota features associated with larval fitness.
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spelling pubmed-84217762021-09-08 Dietary Exposure of Pacific Oyster (Crassostrea gigas) Larvae to Compromised Microalgae Results in Impaired Fitness and Microbiome Shift Vignier, Julien Laroche, Olivier Rolton, Anne Wadsworth, Pandora Kumanan, Karthiga Trochel, Branwen Pochon, Xavier King, Nick Front Microbiol Microbiology The Pacific oyster Crassostrea gigas is the world’s most cultivated oyster and seed supply is heavily reliant on hatchery production where recurring mass mortality events are a major constraint. Outbreaks of bacterial infection via microalgal feed are frequently implicated in these mortalities. This study assessed the effects of feeding compromised microalgae to developing oyster larvae. Intentionally ‘stressed’ (high pH) or non-stressed microalgae were fed to 11 day-old oyster larvae at two feeding rations for 96 h, followed by a recovery period. Biological endpoints of larval performance were measured following the 96 h exposure and subsequent recovery. Bacterial communities associated with the microalgae feed, rearing seawater, and the oyster larvae, were characterized and correlated with effects on oyster fitness parameters. Feeding stressed algae to oyster larvae for 96 h increased the occurrence of deformities (>70% vs. 20% in control), reduced feeding and swimming ability, and slowed development. Following the recovery period, fewer larvae reached pediveliger stage (2.7% vs. 36% in control) and became spat (1.5% vs. 6.6% in control). The quantity of stressed algae supplied to oyster larvae also influenced overall larval performance, with high feeding rations generally causing greater impairment than low rations. Bacterial profiling using 16S rRNA showed that most bacterial families characterized in larval tissue were also present in larval rearing seawater and in the microalgae feed (98%). The rearing seawater showed the highest bacterial richness compared to the larval and the microalgal compartments, regardless of feeding regime. In larval tissue, bacterial richness was highest in stressed and high-feed treatments, and negatively correlated with larval fitness parameters. These results suggest significant dysbiosis induced by compromised feed and/or increased feed ration. Several bacterial genera (e.g., Halomonas, Marinomonas) were strongly associated with impaired larval performance while the presence of genera in larvae including Vibrio was closely associated with overfeeding. Our research demonstrated that metabarcoding can be effectively used to identify microbiota features associated with larval fitness. Frontiers Media S.A. 2021-08-24 /pmc/articles/PMC8421776/ /pubmed/34504478 http://dx.doi.org/10.3389/fmicb.2021.706214 Text en Copyright © 2021 Vignier, Laroche, Rolton, Wadsworth, Kumanan, Trochel, Pochon and King. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Vignier, Julien
Laroche, Olivier
Rolton, Anne
Wadsworth, Pandora
Kumanan, Karthiga
Trochel, Branwen
Pochon, Xavier
King, Nick
Dietary Exposure of Pacific Oyster (Crassostrea gigas) Larvae to Compromised Microalgae Results in Impaired Fitness and Microbiome Shift
title Dietary Exposure of Pacific Oyster (Crassostrea gigas) Larvae to Compromised Microalgae Results in Impaired Fitness and Microbiome Shift
title_full Dietary Exposure of Pacific Oyster (Crassostrea gigas) Larvae to Compromised Microalgae Results in Impaired Fitness and Microbiome Shift
title_fullStr Dietary Exposure of Pacific Oyster (Crassostrea gigas) Larvae to Compromised Microalgae Results in Impaired Fitness and Microbiome Shift
title_full_unstemmed Dietary Exposure of Pacific Oyster (Crassostrea gigas) Larvae to Compromised Microalgae Results in Impaired Fitness and Microbiome Shift
title_short Dietary Exposure of Pacific Oyster (Crassostrea gigas) Larvae to Compromised Microalgae Results in Impaired Fitness and Microbiome Shift
title_sort dietary exposure of pacific oyster (crassostrea gigas) larvae to compromised microalgae results in impaired fitness and microbiome shift
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8421776/
https://www.ncbi.nlm.nih.gov/pubmed/34504478
http://dx.doi.org/10.3389/fmicb.2021.706214
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