Prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species

International audience The role of microbiota in health and disease is most often expressed by structural shifts of the taxonomic composition of prokaryote communities in infected and healthy individuals. In cultured aquatic animals with open circulatory systems, such as mollusks, microbiota also ha...

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Published in:Aquaculture
Main Authors: Wegner, K. Mathias, Morga, Benjamin, Guillou, Laure, Strittmatter, Martina, Lecadet, Cyrielle, Travers, Marie-Agnes, Tourbiez, Delphine, Gervais, Ophélie, Arzul, Isabelle
Other Authors: Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung = Alfred Wegener Institute for Polar and Marine Research = Institut Alfred-Wegener pour la recherche polaire et marine (AWI), Helmholtz-Gemeinschaft = Helmholtz Association, Unité Santé, Génétique et Microbiologie des Mollusques (SGMM), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER), ECOlogy of MArine Plankton (ECOMAP), Adaptation et diversité en milieu marin (ADMM), Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Interactions Hôtes-Pathogènes-Environnements (IHPE), Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 1482
Subjects:
Online Access:https://hal.science/hal-04665295
https://hal.science/hal-04665295/document
https://hal.science/hal-04665295/file/Wegner-2024-Aquaculture-Prokaryotip-MANUSCRIT.pdf
https://doi.org/10.1016/j.aquaculture.2024.741363
id ftunivperpignan:oai:HAL:hal-04665295v1
record_format openpolar
institution Open Polar
collection Université de Perpignan: HAL
op_collection_id ftunivperpignan
language English
topic Microbiome
16s rRNA 18s rRNA amplicon sequencing
mollusk
bivalve
probiotic
[SDV.BA.MVSA]Life Sciences [q-bio]/Animal biology/Veterinary medicine and animal Health
[SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies
spellingShingle Microbiome
16s rRNA 18s rRNA amplicon sequencing
mollusk
bivalve
probiotic
[SDV.BA.MVSA]Life Sciences [q-bio]/Animal biology/Veterinary medicine and animal Health
[SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies
Wegner, K. Mathias
Morga, Benjamin
Guillou, Laure
Strittmatter, Martina
Lecadet, Cyrielle
Travers, Marie-Agnes
Tourbiez, Delphine
Gervais, Ophélie
Arzul, Isabelle
Prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species
topic_facet Microbiome
16s rRNA 18s rRNA amplicon sequencing
mollusk
bivalve
probiotic
[SDV.BA.MVSA]Life Sciences [q-bio]/Animal biology/Veterinary medicine and animal Health
[SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies
description International audience The role of microbiota in health and disease is most often expressed by structural shifts of the taxonomic composition of prokaryote communities in infected and healthy individuals. In cultured aquatic animals with open circulatory systems, such as mollusks, microbiota also harbor a wide range of protists, which are unicellular eukaryotes that could also play an important role during infections. To evaluate the effectiveness of eukaryotic vs. prokaryotic microbiota in characterizing infection states, we examined both microbial compartments under natural conditions in two commercially important oyster species, the flat oyster Ostrea edulis and the Pacific oyster Magallana (Crassostrea) gigas. With O. edulis being infected by two protist parasites, Marteilia refringens and Bonamia ostreae, and M. gigas being infected by the ostreid herpes virus OsHV-1, we chose iconic diseases responsible for substantial mortalities and economic damage within the two species. We analyzed and compared the structural and compositional differences between healthy and infected oysters and used random forest machine learning to classify infection states and identify indicator taxa that distinguish healthy from infected individuals. Both at the structural and compositional levels, bacterial microbiota proved to be better predictors of infection states. By eliminating noisy taxa through variable selection in the random forest models, we enhanced the compositional differences between infection states. In all host-pathogen combinations, only a few taxa (<31) were required to achieve optimal separation. While the identity of indicator taxa will partly reflect the specific environmental conditions at the time of sampling, we recovered several previously described indicator taxa, such as Mycoplasma, Vibrio, Photobacterium, and Arcobacter. Next to these we also discovered new taxa like Motiliproteus that exhibited the potential to differentiate between infection states of the investigated O. edulis specimen. The ...
author2 Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung = Alfred Wegener Institute for Polar and Marine Research = Institut Alfred-Wegener pour la recherche polaire et marine (AWI)
Helmholtz-Gemeinschaft = Helmholtz Association
Unité Santé, Génétique et Microbiologie des Mollusques (SGMM)
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)
ECOlogy of MArine Plankton (ECOMAP)
Adaptation et diversité en milieu marin (ADMM)
Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR)
Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR)
Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)
Interactions Hôtes-Pathogènes-Environnements (IHPE)
Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)
format Article in Journal/Newspaper
author Wegner, K. Mathias
Morga, Benjamin
Guillou, Laure
Strittmatter, Martina
Lecadet, Cyrielle
Travers, Marie-Agnes
Tourbiez, Delphine
Gervais, Ophélie
Arzul, Isabelle
author_facet Wegner, K. Mathias
Morga, Benjamin
Guillou, Laure
Strittmatter, Martina
Lecadet, Cyrielle
Travers, Marie-Agnes
Tourbiez, Delphine
Gervais, Ophélie
Arzul, Isabelle
author_sort Wegner, K. Mathias
title Prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species
title_short Prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species
title_full Prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species
title_fullStr Prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species
title_full_unstemmed Prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species
title_sort prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species
publisher HAL CCSD
publishDate 1482
url https://hal.science/hal-04665295
https://hal.science/hal-04665295/document
https://hal.science/hal-04665295/file/Wegner-2024-Aquaculture-Prokaryotip-MANUSCRIT.pdf
https://doi.org/10.1016/j.aquaculture.2024.741363
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source ISSN: 0044-8486
EISSN: 1873-5622
Aquaculture
https://hal.science/hal-04665295
Aquaculture, 2025, 594, pp.741363. &#x27E8;10.1016/j.aquaculture.2024.741363&#x27E9;
https://www.sciencedirect.com/science/article/pii/S004484862400824X
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1016/j.aquaculture.2024.741363
hal-04665295
https://hal.science/hal-04665295
https://hal.science/hal-04665295/document
https://hal.science/hal-04665295/file/Wegner-2024-Aquaculture-Prokaryotip-MANUSCRIT.pdf
doi:10.1016/j.aquaculture.2024.741363
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1016/j.aquaculture.2024.741363
container_title Aquaculture
container_volume 594
container_start_page 741363
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spelling ftunivperpignan:oai:HAL:hal-04665295v1 2024-09-15T18:03:19+00:00 Prokaryotic microbiota outperform eukaryotic microbiota in differentiating between infection states of iconic diseases of two commercial oyster species Wegner, K. Mathias Morga, Benjamin Guillou, Laure Strittmatter, Martina Lecadet, Cyrielle Travers, Marie-Agnes Tourbiez, Delphine Gervais, Ophélie Arzul, Isabelle Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung = Alfred Wegener Institute for Polar and Marine Research = Institut Alfred-Wegener pour la recherche polaire et marine (AWI) Helmholtz-Gemeinschaft = Helmholtz Association Unité Santé, Génétique et Microbiologie des Mollusques (SGMM) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) ECOlogy of MArine Plankton (ECOMAP) Adaptation et diversité en milieu marin (ADMM) Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR) Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Station biologique de Roscoff = Roscoff Marine Station (SBR) Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS) Interactions Hôtes-Pathogènes-Environnements (IHPE) Université de Perpignan Via Domitia (UPVD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM) 2025-01 https://hal.science/hal-04665295 https://hal.science/hal-04665295/document https://hal.science/hal-04665295/file/Wegner-2024-Aquaculture-Prokaryotip-MANUSCRIT.pdf https://doi.org/10.1016/j.aquaculture.2024.741363 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.aquaculture.2024.741363 hal-04665295 https://hal.science/hal-04665295 https://hal.science/hal-04665295/document https://hal.science/hal-04665295/file/Wegner-2024-Aquaculture-Prokaryotip-MANUSCRIT.pdf doi:10.1016/j.aquaculture.2024.741363 info:eu-repo/semantics/OpenAccess ISSN: 0044-8486 EISSN: 1873-5622 Aquaculture https://hal.science/hal-04665295 Aquaculture, 2025, 594, pp.741363. &#x27E8;10.1016/j.aquaculture.2024.741363&#x27E9; https://www.sciencedirect.com/science/article/pii/S004484862400824X Microbiome 16s rRNA 18s rRNA amplicon sequencing mollusk bivalve probiotic [SDV.BA.MVSA]Life Sciences [q-bio]/Animal biology/Veterinary medicine and animal Health [SDV.SA.SPA]Life Sciences [q-bio]/Agricultural sciences/Animal production studies info:eu-repo/semantics/article Journal articles 1482 ftunivperpignan https://doi.org/10.1016/j.aquaculture.2024.741363 2024-08-06T23:35:16Z International audience The role of microbiota in health and disease is most often expressed by structural shifts of the taxonomic composition of prokaryote communities in infected and healthy individuals. In cultured aquatic animals with open circulatory systems, such as mollusks, microbiota also harbor a wide range of protists, which are unicellular eukaryotes that could also play an important role during infections. To evaluate the effectiveness of eukaryotic vs. prokaryotic microbiota in characterizing infection states, we examined both microbial compartments under natural conditions in two commercially important oyster species, the flat oyster Ostrea edulis and the Pacific oyster Magallana (Crassostrea) gigas. With O. edulis being infected by two protist parasites, Marteilia refringens and Bonamia ostreae, and M. gigas being infected by the ostreid herpes virus OsHV-1, we chose iconic diseases responsible for substantial mortalities and economic damage within the two species. We analyzed and compared the structural and compositional differences between healthy and infected oysters and used random forest machine learning to classify infection states and identify indicator taxa that distinguish healthy from infected individuals. Both at the structural and compositional levels, bacterial microbiota proved to be better predictors of infection states. By eliminating noisy taxa through variable selection in the random forest models, we enhanced the compositional differences between infection states. In all host-pathogen combinations, only a few taxa (<31) were required to achieve optimal separation. While the identity of indicator taxa will partly reflect the specific environmental conditions at the time of sampling, we recovered several previously described indicator taxa, such as Mycoplasma, Vibrio, Photobacterium, and Arcobacter. Next to these we also discovered new taxa like Motiliproteus that exhibited the potential to differentiate between infection states of the investigated O. edulis specimen. The ... Article in Journal/Newspaper Crassostrea gigas Pacific oyster Université de Perpignan: HAL Aquaculture 594 741363