Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota

Type Article
Date 2022-12
Language English
Author(s) de San Nicolas Noémie9, Asokan Aromal2, Rosa Rafael D.ORCID3, Voisin Sébastien N.ORCID4, Travers AgnesORCID1, Rocha Gustavo3, Dantan LucORCID9, Dorant Yann1, Mitta GuillaumeORCID1, 5, Petton BrunoORCID6, Charrière Guillaume M.ORCID9, Escoubas Jean Michel10, Boulo VivianeORCID9, Pouzadoux Juliette9, Meudal HervéORCID2, Loth Karine2, 7, Aucagne VincentORCID2, Delmas Agnès F.2, Bulet PhilippeORCID4, 8, Montagnani CarolineORCID1, Destoumieux Garzon Delphine10
Affiliation(s) 1 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, 34090 Montpellier, France
2 : Centre de Biophysique Moléculaire UPR4301 CNRS, 45071 Orléans, France
3 : Laboratory of Immunology Applied to Aquaculture, Department of Cell Biology, Embryology and Genetics, Federal University of Santa Catarina, 88040-900 Florianópolis, Santa Catarina, Brazil
4 : Plateforme BioPark d’Archamps, Archparc, 74160 Archamps, France
5 : Ifremer, IRD, ILM, Université de Polynésie Française, UMR EIO, 98179 Vairao, French Polynesia
6 : Ifremer, CNRS, IRD, Ifremer, LEMAR UMR 6539 Université de Bretagne Occidentale, 29840 Argenton-en-Landunvez, France
7 : UFR ST, Université d’Orléans, 45067 Orléans, France
8 : CR UGA, IAB, INSERM U1209, CNRS UMR5309, 74160 La Tronche-Archamps, France
9 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, 34090 Montpellier, France
10 : IHPE, Univ. Montpellier, CNRS, Ifremer, Univ. Perpignan Via Domitia, 34090 Montpellier, France
Source Marine Drugs (1660-3397) (MDPI AG), 2022-12 , Vol. 20 , N. 12 , P. 745 (18p.)
DOI 10.3390/md20120745
WOS© Times Cited 1
Note This article belongs to the Special Issue Marine Proteomics in Exploring Bioactive Peptides and Proteins This is an early access version, the complete PDF, HTML, and XML versions will be available soon.
Keyword(s) antibacterial peptide, beta defensin, diversity, evolution, microbiome, invertebrate, mollusk
Abstract

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.

Full Text
File Pages Size Access
Publisher's official version 18 1 MB Open access
Supplementary material 1 MB Open access
Top of the page

How to cite 

de San Nicolas Noémie, Asokan Aromal, Rosa Rafael D., Voisin Sébastien N., Travers Agnes, Rocha Gustavo, Dantan Luc, Dorant Yann, Mitta Guillaume, Petton Bruno, Charrière Guillaume M., Escoubas Jean Michel, Boulo Viviane, Pouzadoux Juliette, Meudal Hervé, Loth Karine, Aucagne Vincent, Delmas Agnès F., Bulet Philippe, Montagnani Caroline, Destoumieux Garzon Delphine (2022). Functional Diversification of Oyster Big Defensins Generates Antimicrobial Specificity and Synergy against Members of the Microbiota. Marine Drugs, 20(12), 745 (18p.). Publisher's official version : https://doi.org/10.3390/md20120745 , Open Access version : https://archimer.ifremer.fr/doc/00807/91932/