Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota
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....
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ftmdpi:oai:mdpi.com:/1660-3397/20/12/745/ 2023-08-20T04:06:05+02:00 Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota Noémie De San Nicolas Aromal Asokan Rafael D. Rosa Sébastien N. Voisin Marie-Agnès Travers Gustavo Rocha Luc Dantan Yann Dorant Guillaume Mitta Bruno Petton Guillaume M. Charrière Jean-Michel Escoubas Viviane Boulo Juliette Pouzadoux Hervé Meudal Karine Loth Vincent Aucagne Agnès F. Delmas Philippe Bulet Caroline Montagnani Delphine Destoumieux-Garzón agris 2022-11-26 application/pdf https://doi.org/10.3390/md20120745 EN eng Multidisciplinary Digital Publishing Institute https://dx.doi.org/10.3390/md20120745 https://creativecommons.org/licenses/by/4.0/ Marine Drugs; Volume 20; Issue 12; Pages: 745 antibacterial peptide beta defensin diversity evolution microbiome invertebrate mollusk Text 2022 ftmdpi https://doi.org/10.3390/md20120745 2023-08-01T07:31:48Z 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. Text Crassostrea gigas Pacific oyster MDPI Open Access Publishing Pacific Marine Drugs 20 12 745 |
institution |
Open Polar |
collection |
MDPI Open Access Publishing |
op_collection_id |
ftmdpi |
language |
English |
topic |
antibacterial peptide beta defensin diversity evolution microbiome invertebrate mollusk |
spellingShingle |
antibacterial peptide beta defensin diversity evolution microbiome invertebrate mollusk Noémie De San Nicolas Aromal Asokan Rafael D. Rosa Sébastien N. Voisin Marie-Agnès Travers Gustavo Rocha Luc Dantan Yann Dorant Guillaume Mitta Bruno Petton Guillaume M. Charrière Jean-Michel Escoubas Viviane Boulo Juliette Pouzadoux Hervé Meudal Karine Loth Vincent Aucagne Agnès F. Delmas Philippe Bulet Caroline Montagnani Delphine Destoumieux-Garzón Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota |
topic_facet |
antibacterial peptide beta defensin diversity evolution microbiome invertebrate mollusk |
description |
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. |
format |
Text |
author |
Noémie De San Nicolas Aromal Asokan Rafael D. Rosa Sébastien N. Voisin Marie-Agnès Travers Gustavo Rocha Luc Dantan Yann Dorant Guillaume Mitta Bruno Petton Guillaume M. Charrière Jean-Michel Escoubas Viviane Boulo Juliette Pouzadoux Hervé Meudal Karine Loth Vincent Aucagne Agnès F. Delmas Philippe Bulet Caroline Montagnani Delphine Destoumieux-Garzón |
author_facet |
Noémie De San Nicolas Aromal Asokan Rafael D. Rosa Sébastien N. Voisin Marie-Agnès Travers Gustavo Rocha Luc Dantan Yann Dorant Guillaume Mitta Bruno Petton Guillaume M. Charrière Jean-Michel Escoubas Viviane Boulo Juliette Pouzadoux Hervé Meudal Karine Loth Vincent Aucagne Agnès F. Delmas Philippe Bulet Caroline Montagnani Delphine Destoumieux-Garzón |
author_sort |
Noémie De San Nicolas |
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 |
Multidisciplinary Digital Publishing Institute |
publishDate |
2022 |
url |
https://doi.org/10.3390/md20120745 |
op_coverage |
agris |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
Marine Drugs; Volume 20; Issue 12; Pages: 745 |
op_relation |
https://dx.doi.org/10.3390/md20120745 |
op_rights |
https://creativecommons.org/licenses/by/4.0/ |
op_doi |
https://doi.org/10.3390/md20120745 |
container_title |
Marine Drugs |
container_volume |
20 |
container_issue |
12 |
container_start_page |
745 |
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1774716994056093696 |