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Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival

Aquacultured animals are reared in water, where they interact with microorganisms which can be involved in their development, immunity, and disease. It is therefore interesting to study the rearing water microbiota, especially in the hatcheries of the Pacific blue shrimp Penaeus stylirostris, where...

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Autores principales: Callac, Nolwenn, Boulo, Viviane, Giraud, Carolane, Beauvais, Maxime, Ansquer, Dominique, Ballan, Valentine, Maillez, Jean-René, Wabete, Nelly, Pham, Dominique
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769815/
https://www.ncbi.nlm.nih.gov/pubmed/36416556
http://dx.doi.org/10.1128/spectrum.04241-22
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author Callac, Nolwenn
Boulo, Viviane
Giraud, Carolane
Beauvais, Maxime
Ansquer, Dominique
Ballan, Valentine
Maillez, Jean-René
Wabete, Nelly
Pham, Dominique
author_facet Callac, Nolwenn
Boulo, Viviane
Giraud, Carolane
Beauvais, Maxime
Ansquer, Dominique
Ballan, Valentine
Maillez, Jean-René
Wabete, Nelly
Pham, Dominique
author_sort Callac, Nolwenn
collection PubMed
description Aquacultured animals are reared in water, where they interact with microorganisms which can be involved in their development, immunity, and disease. It is therefore interesting to study the rearing water microbiota, especially in the hatcheries of the Pacific blue shrimp Penaeus stylirostris, where larval mass mortalities occur. In this study, using HiSeq sequencing of the V4 region of the 16S rRNA molecule coupled with zootechnical and chemical analyses, we investigated whether any microbial lineages could be associated with certain mortality rates at a given larval stage. Our results indicate that the active microbiota of the rearing water was highly dynamic throughout the rearing process, with distinct communities influenced by progressive water eutrophication, larval stage, and survival rate. Our data also highlighted the role of the lagoon seawater on the rearing water microbiome, as many operational taxonomic units (OTUs) specific to a given larval stage and survival rate were detected in the primary reservoir which contained the lagoon water. We also identified biomarkers specific to water eutrophication, with Alteromonadaceae, Vibrionaceae, and Methylophilaceae, respectively, linked to increases in ammonia, nitrogen, and soluble reactive phosphate, or to increases in colored dissolved organic matter in the rearing water; other biomarkers were specific to certain larval stages and survival rates. Indeed, the Marinobacteraceae were specific to the Nauplii, and the Thalassospiraceae and Saprospiraceae to the Zoea Good condition; when mortality occurred, the Litoricolaceae were specific to the Zoea Bad, Microbacteraceae to the Mysis Bad, and Methylophilaceae to the Mysis Worst condition. Thus, these biomarkers might be used as potential early warning sentinels in water storage to infer the evolution of larval rearing to improve shrimp larval rearing. IMPORTANCE In New Caledonia, rearing of P. stylirostris is one of the main economic activities; unfortunately, mass larval mortalities cause important production decreases, involving major economic losses for the farmers and the Territory. This phenomenon, which has occurred at any larval stage over the past decade, is poorly understood. The significance of our research is in the identification of biomarkers specific to larval stage and survival rate, with some of these biomarkers being already present in the lagoon water. This enhances the role of the lagoon on the active microbiota of the rearing water at various larval stages and survival rates. Together, our results help us understand which active microbial communities are present in the rearing water according to larval stage and health. This might lead to broader impacts on hatcheries by helping to develop useful tools for using the water—lagoon, reservoir, or rearing—to test for the presence of these biomarkers as an early monitoring strategy.
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spelling pubmed-97698152022-12-22 Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival Callac, Nolwenn Boulo, Viviane Giraud, Carolane Beauvais, Maxime Ansquer, Dominique Ballan, Valentine Maillez, Jean-René Wabete, Nelly Pham, Dominique Microbiol Spectr Research Article Aquacultured animals are reared in water, where they interact with microorganisms which can be involved in their development, immunity, and disease. It is therefore interesting to study the rearing water microbiota, especially in the hatcheries of the Pacific blue shrimp Penaeus stylirostris, where larval mass mortalities occur. In this study, using HiSeq sequencing of the V4 region of the 16S rRNA molecule coupled with zootechnical and chemical analyses, we investigated whether any microbial lineages could be associated with certain mortality rates at a given larval stage. Our results indicate that the active microbiota of the rearing water was highly dynamic throughout the rearing process, with distinct communities influenced by progressive water eutrophication, larval stage, and survival rate. Our data also highlighted the role of the lagoon seawater on the rearing water microbiome, as many operational taxonomic units (OTUs) specific to a given larval stage and survival rate were detected in the primary reservoir which contained the lagoon water. We also identified biomarkers specific to water eutrophication, with Alteromonadaceae, Vibrionaceae, and Methylophilaceae, respectively, linked to increases in ammonia, nitrogen, and soluble reactive phosphate, or to increases in colored dissolved organic matter in the rearing water; other biomarkers were specific to certain larval stages and survival rates. Indeed, the Marinobacteraceae were specific to the Nauplii, and the Thalassospiraceae and Saprospiraceae to the Zoea Good condition; when mortality occurred, the Litoricolaceae were specific to the Zoea Bad, Microbacteraceae to the Mysis Bad, and Methylophilaceae to the Mysis Worst condition. Thus, these biomarkers might be used as potential early warning sentinels in water storage to infer the evolution of larval rearing to improve shrimp larval rearing. IMPORTANCE In New Caledonia, rearing of P. stylirostris is one of the main economic activities; unfortunately, mass larval mortalities cause important production decreases, involving major economic losses for the farmers and the Territory. This phenomenon, which has occurred at any larval stage over the past decade, is poorly understood. The significance of our research is in the identification of biomarkers specific to larval stage and survival rate, with some of these biomarkers being already present in the lagoon water. This enhances the role of the lagoon on the active microbiota of the rearing water at various larval stages and survival rates. Together, our results help us understand which active microbial communities are present in the rearing water according to larval stage and health. This might lead to broader impacts on hatcheries by helping to develop useful tools for using the water—lagoon, reservoir, or rearing—to test for the presence of these biomarkers as an early monitoring strategy. American Society for Microbiology 2022-11-23 /pmc/articles/PMC9769815/ /pubmed/36416556 http://dx.doi.org/10.1128/spectrum.04241-22 Text en Copyright © 2022 Callac et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Callac, Nolwenn
Boulo, Viviane
Giraud, Carolane
Beauvais, Maxime
Ansquer, Dominique
Ballan, Valentine
Maillez, Jean-René
Wabete, Nelly
Pham, Dominique
Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival
title Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival
title_full Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival
title_fullStr Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival
title_full_unstemmed Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival
title_short Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival
title_sort microbiota of the rearing water of penaeus stylirostris larvae influenced by lagoon seawater and specific key microbial lineages of larval stage and survival
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9769815/
https://www.ncbi.nlm.nih.gov/pubmed/36416556
http://dx.doi.org/10.1128/spectrum.04241-22
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