Hemolymph microbiota and immune effectors’ expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostris

Abstract Background In holobiont, microbiota is known to play a central role on the health and immunity of its host. Then, understanding the microbiota, its dynamic according to the environmental conditions and its link to the immunity would help to react to potential dysbiosis of aquacultured speci...

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Main Authors: Valérie Perez, Viviane Boulo, Julien De Lorgeril, Dominique Pham, Dominique Ansquer, Gwenola Plougoulen, Valentine Ballan, Jean-Sébastien Lam, Océane Romatif, Jeremy Le Luyer, Corinne Falchetto, Caline Basset, Stanley Flohr, Moana Maamaatuaiahutapu, Marc André Lafille, Christophe Lau, Denis Saulnier, Nelly Wabete, Nolwenn Callac
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Animal Microbiome
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Online Access:https://doi.org/10.1186/s42523-025-00376-1
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author Valérie Perez
Viviane Boulo
Julien De Lorgeril
Dominique Pham
Dominique Ansquer
Gwenola Plougoulen
Valentine Ballan
Jean-Sébastien Lam
Océane Romatif
Jeremy Le Luyer
Corinne Falchetto
Caline Basset
Stanley Flohr
Moana Maamaatuaiahutapu
Marc André Lafille
Christophe Lau
Denis Saulnier
Nelly Wabete
Nolwenn Callac
author_facet Valérie Perez
Viviane Boulo
Julien De Lorgeril
Dominique Pham
Dominique Ansquer
Gwenola Plougoulen
Valentine Ballan
Jean-Sébastien Lam
Océane Romatif
Jeremy Le Luyer
Corinne Falchetto
Caline Basset
Stanley Flohr
Moana Maamaatuaiahutapu
Marc André Lafille
Christophe Lau
Denis Saulnier
Nelly Wabete
Nolwenn Callac
author_sort Valérie Perez
collection DOAJ
description Abstract Background In holobiont, microbiota is known to play a central role on the health and immunity of its host. Then, understanding the microbiota, its dynamic according to the environmental conditions and its link to the immunity would help to react to potential dysbiosis of aquacultured species. While the gut microbiota is highly studied, in marine invertebrates the hemolymph microbiota is often set aside even if it remains an important actor of the hemolymph homeostasis. Indeed, the hemolymph harbors the factors involved in the animal homeostasis that interacts with the microbiota, the immunity. In the Southwest Pacific, the high economical valued shrimp Penaeus stylirostris is reared in two contrasted sites, in New Caledonia (NC) and in French Polynesia (FP). Results We characterized the active microbiota inhabiting the hemolymph of shrimps while considering its stability during two seasons and at a one-month interval and evidenced an important microbial variability between the shrimps according to the rearing conditions and the sites. We highlighted specific biomarkers along with a common core microbiota composed of 6 ASVs. Putative microbial functions were mostly associated with bacterial competition, infections and metabolism in NC, while they were highly associated with the cell metabolism in FP suggesting a rearing site discrimination. Differential relative expression of immune effectors measured in the hemolymph of two shrimp populations from NC and FP, exhibited higher level of expression in NC compared to FP. In addition, differential relative expression of immune effectors was correlated to bacterial biomarkers based on their geographical location. Conclusions Our data suggest that, in Pacific shrimps, both the microbiota and the expression of the immune effectors could have undergone differential immunostimulation according to the rearing site as well as a geographical adaptative divergence of the shrimps as an holobiont, to their rearing sites. Further, the identification of proxies such as the core microbiota and site biomarkers, could be used to guide future actions to monitor the bacterial microbiota and thus preserve the productions.
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spelling doaj-art-6eea8149b60546fcb2af52555210446e2025-01-12T12:41:17ZengBMCAnimal Microbiome2524-46712025-01-017112010.1186/s42523-025-00376-1Hemolymph microbiota and immune effectors’ expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostrisValérie Perez0Viviane Boulo1Julien De Lorgeril2Dominique Pham3Dominique Ansquer4Gwenola Plougoulen5Valentine Ballan6Jean-Sébastien Lam7Océane Romatif8Jeremy Le Luyer9Corinne Falchetto10Caline Basset11Stanley Flohr12Moana Maamaatuaiahutapu13Marc André Lafille14Christophe Lau15Denis Saulnier16Nelly Wabete17Nolwenn Callac18Ifremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEInteractions Hôtes Pathogènes Environnements (IHPE), Université de Montpellier, CNRS, Ifremer, Université de Perpignan Via DomitiaIfremer, Université de la Polynésie Française, ILM, IRD, UMR 241 SECOPOLIfremer, Université de la Polynésie Française, ILM, IRD, UMR 241 SECOPOLIfremer, Université de la Polynésie Française, ILM, IRD, UMR 241 SECOPOLDRM, Direction des Ressources MarinesDRM, Direction des Ressources MarinesDRM, Direction des Ressources MarinesDRM, Direction des Ressources MarinesIfremer, Université de la Polynésie Française, ILM, IRD, UMR 241 SECOPOLIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEIfremer, IRD, Université de la Nouvelle-Calédonie, Université de La Réunion, CNRS, UMR 9220 ENTROPIEAbstract Background In holobiont, microbiota is known to play a central role on the health and immunity of its host. Then, understanding the microbiota, its dynamic according to the environmental conditions and its link to the immunity would help to react to potential dysbiosis of aquacultured species. While the gut microbiota is highly studied, in marine invertebrates the hemolymph microbiota is often set aside even if it remains an important actor of the hemolymph homeostasis. Indeed, the hemolymph harbors the factors involved in the animal homeostasis that interacts with the microbiota, the immunity. In the Southwest Pacific, the high economical valued shrimp Penaeus stylirostris is reared in two contrasted sites, in New Caledonia (NC) and in French Polynesia (FP). Results We characterized the active microbiota inhabiting the hemolymph of shrimps while considering its stability during two seasons and at a one-month interval and evidenced an important microbial variability between the shrimps according to the rearing conditions and the sites. We highlighted specific biomarkers along with a common core microbiota composed of 6 ASVs. Putative microbial functions were mostly associated with bacterial competition, infections and metabolism in NC, while they were highly associated with the cell metabolism in FP suggesting a rearing site discrimination. Differential relative expression of immune effectors measured in the hemolymph of two shrimp populations from NC and FP, exhibited higher level of expression in NC compared to FP. In addition, differential relative expression of immune effectors was correlated to bacterial biomarkers based on their geographical location. Conclusions Our data suggest that, in Pacific shrimps, both the microbiota and the expression of the immune effectors could have undergone differential immunostimulation according to the rearing site as well as a geographical adaptative divergence of the shrimps as an holobiont, to their rearing sites. Further, the identification of proxies such as the core microbiota and site biomarkers, could be used to guide future actions to monitor the bacterial microbiota and thus preserve the productions.https://doi.org/10.1186/s42523-025-00376-1Active microbiotaShrimp hemolymphBiomarkersImmune effectorsHost-microbiota interactionsImmunostimulation
spellingShingle Valérie Perez
Viviane Boulo
Julien De Lorgeril
Dominique Pham
Dominique Ansquer
Gwenola Plougoulen
Valentine Ballan
Jean-Sébastien Lam
Océane Romatif
Jeremy Le Luyer
Corinne Falchetto
Caline Basset
Stanley Flohr
Moana Maamaatuaiahutapu
Marc André Lafille
Christophe Lau
Denis Saulnier
Nelly Wabete
Nolwenn Callac
Hemolymph microbiota and immune effectors’ expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostris
Animal Microbiome
Active microbiota
Shrimp hemolymph
Biomarkers
Immune effectors
Host-microbiota interactions
Immunostimulation
title Hemolymph microbiota and immune effectors’ expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostris
title_full Hemolymph microbiota and immune effectors’ expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostris
title_fullStr Hemolymph microbiota and immune effectors’ expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostris
title_full_unstemmed Hemolymph microbiota and immune effectors’ expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostris
title_short Hemolymph microbiota and immune effectors’ expressions driven by geographical rearing acclimation of the aquacultured Penaeus stylirostris
title_sort hemolymph microbiota and immune effectors expressions driven by geographical rearing acclimation of the aquacultured penaeus stylirostris
topic Active microbiota
Shrimp hemolymph
Biomarkers
Immune effectors
Host-microbiota interactions
Immunostimulation
url https://doi.org/10.1186/s42523-025-00376-1
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