Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota
AMV International audience Big defensins are two-domain antimicrobial peptides (AMPs) that have highly diversified in mollusks. Cg-BigDefs are expressed by immune cells in the oyster Crassostrea gigas, and their expression is dampened during the Pacific Oyster Mortality Syndrome (POMS), which evolve...
Published in: | Marine Drugs |
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Main Authors: | , , , , , , , , , , , , , , , , , , , , |
Other Authors: | , , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2022
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Subjects: | |
Online Access: | https://hal.science/hal-03876842 https://hal.science/hal-03876842/document https://hal.science/hal-03876842/file/marinedrugs-20-00745.pdf https://doi.org/10.3390/md20120745 |
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ftunimontpellier:oai:HAL:hal-03876842v1 |
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openpolar |
institution |
Open Polar |
collection |
Université de Montpellier: HAL |
op_collection_id |
ftunimontpellier |
language |
English |
topic |
[SDE.BE]Environmental Sciences/Biodiversity and Ecology [SDV.BA]Life Sciences [q-bio]/Animal biology [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology |
spellingShingle |
[SDE.BE]Environmental Sciences/Biodiversity and Ecology [SDV.BA]Life Sciences [q-bio]/Animal biology [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology Nicolas, Noémie de San Asokan, Aromal Rosa, Rafael Voisin, Sébastien Travers, Marie-Agnès Rocha, Gustavo Dantan, Luc Dorant, Yann Mitta, Guillaume Petton, Bruno Charrière, Guillaume Escoubas, Jean-Michel Boulo, Viviane Pouzadoux, Juliette Meudal, Hervé Loth, Karine Aucagne, Vincent Delmas, Agnès Bulet, Philippe Montagnani, Caroline Destoumieux-Garzón, Delphine Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota |
topic_facet |
[SDE.BE]Environmental Sciences/Biodiversity and Ecology [SDV.BA]Life Sciences [q-bio]/Animal biology [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology |
description |
AMV International audience Big defensins are two-domain antimicrobial peptides (AMPs) that have highly diversified in mollusks. Cg-BigDefs are expressed by immune cells in the oyster Crassostrea gigas, and their expression is dampened during the Pacific Oyster Mortality Syndrome (POMS), which evolves toward fatal bacteremia. We evaluated whether Cg-BigDefs contribute to the control of oyster-associated microbial communities. Two Cg-BigDefs that are representative of molecular diversity within the peptide family, namely Cg-BigDef1 and Cg-BigDef5, were characterized by gene cloning and synthesized by solid-phase peptide synthesis and native chemical ligation. Synthetic peptides were tested for antibacterial activity against a collection of culturable bacteria belonging to the oyster microbiota, characterized by 16S sequencing and MALDI Biotyping. We first tested the potential of Cg-BigDefs to control the oyster microbiota by injecting synthetic Cg-BigDef1 into oyster tissues and analyzing microbiota dynamics over 24 h by 16S metabarcoding. Cg-BigDef1 induced a significant shift in oyster microbiota β-diversity after 6 h and 24 h, prompting us to investigate antimicrobial activities in vitro against members of the oyster microbiota. Both Cg-BigDef1 and Cg-BigDef5 were active at a high salt concentration (400 mM NaCl) and showed broad spectra of activity against bacteria associated with C. gigas pathologies. Antimicrobial specificity was observed for both molecules at an intra- and inter-genera level. Remarkably, antimicrobial spectra of Cg-BigDef1 and Cg-BigDef5 were complementary, and peptides acted synergistically. Overall, we found that primary sequence diversification of Cg-BigDefs has generated specificity and synergy and extended the spectrum of activity of this peptide family. |
author2 |
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) Centre de biophysique moléculaire (CBM) Université d'Orléans (UO)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS) Universidade Federal de Santa Catarina = Federal University of Santa Catarina Florianópolis (UFSC) BioPark Archamps (BioPark) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Université de la Polynésie Française (UPF) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institute for Advanced Biosciences / Institut pour l'Avancée des Biosciences (Grenoble) (IAB) Centre Hospitalier Universitaire Grenoble (CHU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Etablissement français du sang - Auvergne-Rhône-Alpes (EFS)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA) |
format |
Article in Journal/Newspaper |
author |
Nicolas, Noémie de San Asokan, Aromal Rosa, Rafael Voisin, Sébastien Travers, Marie-Agnès Rocha, Gustavo Dantan, Luc Dorant, Yann Mitta, Guillaume Petton, Bruno Charrière, Guillaume Escoubas, Jean-Michel Boulo, Viviane Pouzadoux, Juliette Meudal, Hervé Loth, Karine Aucagne, Vincent Delmas, Agnès Bulet, Philippe Montagnani, Caroline Destoumieux-Garzón, Delphine |
author_facet |
Nicolas, Noémie de San Asokan, Aromal Rosa, Rafael Voisin, Sébastien Travers, Marie-Agnès Rocha, Gustavo Dantan, Luc Dorant, Yann Mitta, Guillaume Petton, Bruno Charrière, Guillaume Escoubas, Jean-Michel Boulo, Viviane Pouzadoux, Juliette Meudal, Hervé Loth, Karine Aucagne, Vincent Delmas, Agnès Bulet, Philippe Montagnani, Caroline Destoumieux-Garzón, Delphine |
author_sort |
Nicolas, Noémie de San |
title |
Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota |
title_short |
Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota |
title_full |
Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota |
title_fullStr |
Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota |
title_full_unstemmed |
Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota |
title_sort |
functional diversification of oyster big defensins generates antimicrobial specificity and synergy against members of the microbiota |
publisher |
HAL CCSD |
publishDate |
2022 |
url |
https://hal.science/hal-03876842 https://hal.science/hal-03876842/document https://hal.science/hal-03876842/file/marinedrugs-20-00745.pdf https://doi.org/10.3390/md20120745 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
ISSN: 1660-3397 Marine drugs https://hal.science/hal-03876842 Marine drugs, 2022, 20 (12), pp.745. ⟨10.3390/md20120745⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.3390/md20120745 hal-03876842 https://hal.science/hal-03876842 https://hal.science/hal-03876842/document https://hal.science/hal-03876842/file/marinedrugs-20-00745.pdf doi:10.3390/md20120745 |
op_rights |
http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.3390/md20120745 |
container_title |
Marine Drugs |
container_volume |
20 |
container_issue |
12 |
container_start_page |
745 |
_version_ |
1785581576956936192 |
spelling |
ftunimontpellier:oai:HAL:hal-03876842v1 2023-12-17T10:29:15+01:00 Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota Nicolas, Noémie de San Asokan, Aromal Rosa, Rafael Voisin, Sébastien Travers, Marie-Agnès Rocha, Gustavo Dantan, Luc Dorant, Yann Mitta, Guillaume Petton, Bruno Charrière, Guillaume Escoubas, Jean-Michel Boulo, Viviane Pouzadoux, Juliette Meudal, Hervé Loth, Karine Aucagne, Vincent Delmas, Agnès Bulet, Philippe Montagnani, Caroline Destoumieux-Garzón, Delphine 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) Centre de biophysique moléculaire (CBM) Université d'Orléans (UO)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut de Chimie - CNRS Chimie (INC-CNRS)-Centre National de la Recherche Scientifique (CNRS) Universidade Federal de Santa Catarina = Federal University of Santa Catarina Florianópolis (UFSC) BioPark Archamps (BioPark) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Université de la Polynésie Française (UPF) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institute for Advanced Biosciences / Institut pour l'Avancée des Biosciences (Grenoble) (IAB) Centre Hospitalier Universitaire Grenoble (CHU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Etablissement français du sang - Auvergne-Rhône-Alpes (EFS)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA) 2022-12 https://hal.science/hal-03876842 https://hal.science/hal-03876842/document https://hal.science/hal-03876842/file/marinedrugs-20-00745.pdf https://doi.org/10.3390/md20120745 en eng HAL CCSD MDPI info:eu-repo/semantics/altIdentifier/doi/10.3390/md20120745 hal-03876842 https://hal.science/hal-03876842 https://hal.science/hal-03876842/document https://hal.science/hal-03876842/file/marinedrugs-20-00745.pdf doi:10.3390/md20120745 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1660-3397 Marine drugs https://hal.science/hal-03876842 Marine drugs, 2022, 20 (12), pp.745. ⟨10.3390/md20120745⟩ [SDE.BE]Environmental Sciences/Biodiversity and Ecology [SDV.BA]Life Sciences [q-bio]/Animal biology [SDV.BBM]Life Sciences [q-bio]/Biochemistry Molecular Biology info:eu-repo/semantics/article Journal articles 2022 ftunimontpellier https://doi.org/10.3390/md20120745 2023-11-21T23:36:35Z AMV International audience Big defensins are two-domain antimicrobial peptides (AMPs) that have highly diversified in mollusks. Cg-BigDefs are expressed by immune cells in the oyster Crassostrea gigas, and their expression is dampened during the Pacific Oyster Mortality Syndrome (POMS), which evolves toward fatal bacteremia. We evaluated whether Cg-BigDefs contribute to the control of oyster-associated microbial communities. Two Cg-BigDefs that are representative of molecular diversity within the peptide family, namely Cg-BigDef1 and Cg-BigDef5, were characterized by gene cloning and synthesized by solid-phase peptide synthesis and native chemical ligation. Synthetic peptides were tested for antibacterial activity against a collection of culturable bacteria belonging to the oyster microbiota, characterized by 16S sequencing and MALDI Biotyping. We first tested the potential of Cg-BigDefs to control the oyster microbiota by injecting synthetic Cg-BigDef1 into oyster tissues and analyzing microbiota dynamics over 24 h by 16S metabarcoding. Cg-BigDef1 induced a significant shift in oyster microbiota β-diversity after 6 h and 24 h, prompting us to investigate antimicrobial activities in vitro against members of the oyster microbiota. Both Cg-BigDef1 and Cg-BigDef5 were active at a high salt concentration (400 mM NaCl) and showed broad spectra of activity against bacteria associated with C. gigas pathologies. Antimicrobial specificity was observed for both molecules at an intra- and inter-genera level. Remarkably, antimicrobial spectra of Cg-BigDef1 and Cg-BigDef5 were complementary, and peptides acted synergistically. Overall, we found that primary sequence diversification of Cg-BigDefs has generated specificity and synergy and extended the spectrum of activity of this peptide family. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Université de Montpellier: HAL Pacific Marine Drugs 20 12 745 |