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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MDPI AG
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Online Access: | https://doi.org/10.3390/md20120745 https://doaj.org/article/4923b5562d554c37a634ea0a302333bf |
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ftdoajarticles:oai:doaj.org/article:4923b5562d554c37a634ea0a302333bf 2023-05-15T15:58:56+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 2022-11-01T00:00:00Z https://doi.org/10.3390/md20120745 https://doaj.org/article/4923b5562d554c37a634ea0a302333bf EN eng MDPI AG https://www.mdpi.com/1660-3397/20/12/745 https://doaj.org/toc/1660-3397 doi:10.3390/md20120745 1660-3397 https://doaj.org/article/4923b5562d554c37a634ea0a302333bf Marine Drugs, Vol 20, Iss 745, p 745 (2022) antibacterial peptide beta defensin diversity evolution microbiome invertebrate Biology (General) QH301-705.5 article 2022 ftdoajarticles https://doi.org/10.3390/md20120745 2022-12-30T19:31:11Z 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 Directory of Open Access Journals: DOAJ Articles Pacific Marine Drugs 20 12 745 |
institution |
Open Polar |
collection |
Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
antibacterial peptide beta defensin diversity evolution microbiome invertebrate Biology (General) QH301-705.5 |
spellingShingle |
antibacterial peptide beta defensin diversity evolution microbiome invertebrate Biology (General) QH301-705.5 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 Biology (General) QH301-705.5 |
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 |
Article in Journal/Newspaper |
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 |
MDPI AG |
publishDate |
2022 |
url |
https://doi.org/10.3390/md20120745 https://doaj.org/article/4923b5562d554c37a634ea0a302333bf |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
Marine Drugs, Vol 20, Iss 745, p 745 (2022) |
op_relation |
https://www.mdpi.com/1660-3397/20/12/745 https://doaj.org/toc/1660-3397 doi:10.3390/md20120745 1660-3397 https://doaj.org/article/4923b5562d554c37a634ea0a302333bf |
op_doi |
https://doi.org/10.3390/md20120745 |
container_title |
Marine Drugs |
container_volume |
20 |
container_issue |
12 |
container_start_page |
745 |
_version_ |
1766394719107022848 |