Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival
ABSTRACT 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 stylirostri...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2022-12-01
|
| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.04241-22 |
| _version_ | 1797979761747689472 |
|---|---|
| author | Nolwenn Callac Viviane Boulo Carolane Giraud Maxime Beauvais Dominique Ansquer Valentine Ballan Jean-René Maillez Nelly Wabete Dominique Pham |
| author_facet | Nolwenn Callac Viviane Boulo Carolane Giraud Maxime Beauvais Dominique Ansquer Valentine Ballan Jean-René Maillez Nelly Wabete Dominique Pham |
| author_sort | Nolwenn Callac |
| collection | DOAJ |
| description | ABSTRACT 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. |
| first_indexed | 2024-04-11T05:43:49Z |
| format | Article |
| id | doaj.art-b6de6f69cd254fd293be7ac20219836b |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-11T05:43:49Z |
| publishDate | 2022-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-b6de6f69cd254fd293be7ac20219836b2022-12-22T04:42:20ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-12-0110610.1128/spectrum.04241-22Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and SurvivalNolwenn Callac0Viviane Boulo1Carolane Giraud2Maxime Beauvais3Dominique Ansquer4Valentine Ballan5Jean-René Maillez6Nelly Wabete7Dominique Pham8Ifremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaABSTRACT 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.https://journals.asm.org/doi/10.1128/spectrum.04241-22active microbiotarearing watercore microbiomespecific microbiomelarvaeshrimp |
| spellingShingle | Nolwenn Callac Viviane Boulo Carolane Giraud Maxime Beauvais Dominique Ansquer Valentine Ballan Jean-René Maillez Nelly Wabete Dominique Pham Microbiota of the Rearing Water of Penaeus stylirostris Larvae Influenced by Lagoon Seawater and Specific Key Microbial Lineages of Larval Stage and Survival Microbiology Spectrum active microbiota rearing water core microbiome specific microbiome larvae shrimp |
| 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 | active microbiota rearing water core microbiome specific microbiome larvae shrimp |
| url | https://journals.asm.org/doi/10.1128/spectrum.04241-22 |
| work_keys_str_mv | AT nolwenncallac microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival AT vivianeboulo microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival AT carolanegiraud microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival AT maximebeauvais microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival AT dominiqueansquer microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival AT valentineballan microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival AT jeanrenemaillez microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival AT nellywabete microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival AT dominiquepham microbiotaoftherearingwaterofpenaeusstylirostrislarvaeinfluencedbylagoonseawaterandspecifickeymicrobiallineagesoflarvalstageandsurvival |