Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response
Mass mortality events caused by vibriosis have emerged in hatchery-reared scallop larvae from Chile, threatening scallop aquaculture. In an attempt to mitigate this emerging infectious disease and provide candidates for marker-assisted selective breeding, we tested here the existence of a genetic co...
| Main Authors: | , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-03-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1150280/full |
| _version_ | 1811160833491730432 |
|---|---|
| author | Eduardo Jeria Daniel Oyanedel Rodrigo Rojas Rodolfo Farlora Rodolfo Farlora German Lira Ana Mercado Katherine Muñoz Delphine Destoumieux-Garzón Katherina Brokordt Paulina Schmitt |
| author_facet | Eduardo Jeria Daniel Oyanedel Rodrigo Rojas Rodolfo Farlora Rodolfo Farlora German Lira Ana Mercado Katherine Muñoz Delphine Destoumieux-Garzón Katherina Brokordt Paulina Schmitt |
| author_sort | Eduardo Jeria |
| collection | DOAJ |
| description | Mass mortality events caused by vibriosis have emerged in hatchery-reared scallop larvae from Chile, threatening scallop aquaculture. In an attempt to mitigate this emerging infectious disease and provide candidates for marker-assisted selective breeding, we tested here the existence of a genetic component of Argopecten purpuratus scallop resistance to the pathogen Vibrio bivalvicida. Through a dual RNA-seq approach we analyzed the basal transcriptome and the transcriptional response to infection in two resistant and two susceptible families as well as the pathogen transcriptomic response to host colonization. The results highlighted a genetic basis in the resistance of scallop larvae to the pathogen. The Vibrio response was characterized by a general metabolic adaptation to the host environment, along with several predicted virulence factors overexpressed in infected scallop larvae with no difference between resistant and susceptible host phenotypes. On the host side, several biological processes were enriched in uninfected resistant larvae. Within these enriched categories, immune-related processes were overexpressed, while morphogenesis, biomineral tissue development, and angiogenesis were under expressed. Particularly, genes involved in immune recognition and antimicrobial response, such as lipopolysaccharide-binding proteins (LBPs), lysozyme, and bactericidal permeability-increasing protein (BPI) were overexpressed in uninfected resistant larvae. As expected, immune-related biological processes were enriched in Vibrio-infected larvae, but they were more numerous in resistant larvae. Overexpressed immune genes in response to infection included several Toll-like receptors, TNF and NF-κB immune signaling genes, and the antimicrobial peptide Big defensin ApBD1. Results strongly suggest that both a front-loading of immune genes and an enhanced antimicrobial response to infection contribute to the resistance, while pathogen infective strategy does not discriminate between host phenotypes. Overall, early expression of host immune genes appears as a strong determinant of the disease outcome that could be used in marker-assisted selective breeding. |
| first_indexed | 2024-04-10T06:04:16Z |
| format | Article |
| id | doaj.art-c6fcdb94921047d78f7059719c831fae |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-10T06:04:16Z |
| publishDate | 2023-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-c6fcdb94921047d78f7059719c831fae2023-03-03T05:13:02ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-03-011410.3389/fimmu.2023.11502801150280Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial responseEduardo Jeria0Daniel Oyanedel1Rodrigo Rojas2Rodolfo Farlora3Rodolfo Farlora4German Lira5Ana Mercado6Katherine Muñoz7Delphine Destoumieux-Garzón8Katherina Brokordt9Paulina Schmitt10Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, ChileLaboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, ChileLaboratorio de Patobiología Acuática, Departamento de Acuicultura, Universidad Católica del Norte, Coquimbo, ChileLaboratorio de Biotecnología Acuática y Genómica Reproductiva (LABYGER), Instituto de Biología, Facultad de Ciencias, Universidad de Valparaíso, Valparaíso, ChileCentro de Investigación y Gestión de Recursos Naturales (CIGREN), Universidad de Valparaíso, Valparaíso, ChileLaboratorio de Fisiología y Genética Marina (FIGEMA), Departamento de Acuicultura, Universidad Católica del Norte, Coquimbo, ChileLaboratorio de Fisiología y Genética Marina (FIGEMA), Departamento de Acuicultura, Universidad Católica del Norte, Coquimbo, ChileLaboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, ChileIHPE, Université de Montpellier, CNRS, Ifremer, Université de Perpignan Via Domitia, Montpellier, FranceLaboratorio de Fisiología y Genética Marina (FIGEMA), Departamento de Acuicultura, Universidad Católica del Norte, Coquimbo, ChileLaboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, ChileMass mortality events caused by vibriosis have emerged in hatchery-reared scallop larvae from Chile, threatening scallop aquaculture. In an attempt to mitigate this emerging infectious disease and provide candidates for marker-assisted selective breeding, we tested here the existence of a genetic component of Argopecten purpuratus scallop resistance to the pathogen Vibrio bivalvicida. Through a dual RNA-seq approach we analyzed the basal transcriptome and the transcriptional response to infection in two resistant and two susceptible families as well as the pathogen transcriptomic response to host colonization. The results highlighted a genetic basis in the resistance of scallop larvae to the pathogen. The Vibrio response was characterized by a general metabolic adaptation to the host environment, along with several predicted virulence factors overexpressed in infected scallop larvae with no difference between resistant and susceptible host phenotypes. On the host side, several biological processes were enriched in uninfected resistant larvae. Within these enriched categories, immune-related processes were overexpressed, while morphogenesis, biomineral tissue development, and angiogenesis were under expressed. Particularly, genes involved in immune recognition and antimicrobial response, such as lipopolysaccharide-binding proteins (LBPs), lysozyme, and bactericidal permeability-increasing protein (BPI) were overexpressed in uninfected resistant larvae. As expected, immune-related biological processes were enriched in Vibrio-infected larvae, but they were more numerous in resistant larvae. Overexpressed immune genes in response to infection included several Toll-like receptors, TNF and NF-κB immune signaling genes, and the antimicrobial peptide Big defensin ApBD1. Results strongly suggest that both a front-loading of immune genes and an enhanced antimicrobial response to infection contribute to the resistance, while pathogen infective strategy does not discriminate between host phenotypes. Overall, early expression of host immune genes appears as a strong determinant of the disease outcome that could be used in marker-assisted selective breeding.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1150280/fullmolluskscallop-Vibrio interactioninvertebrate immunityimmune front-loadingresistance to diseases |
| spellingShingle | Eduardo Jeria Daniel Oyanedel Rodrigo Rojas Rodolfo Farlora Rodolfo Farlora German Lira Ana Mercado Katherine Muñoz Delphine Destoumieux-Garzón Katherina Brokordt Paulina Schmitt Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response Frontiers in Immunology mollusk scallop-Vibrio interaction invertebrate immunity immune front-loading resistance to diseases |
| title | Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response |
| title_full | Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response |
| title_fullStr | Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response |
| title_full_unstemmed | Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response |
| title_short | Resistance of Argopecten purpuratus scallop larvae to vibriosis is associated with the front-loading of immune genes and enhanced antimicrobial response |
| title_sort | resistance of argopecten purpuratus scallop larvae to vibriosis is associated with the front loading of immune genes and enhanced antimicrobial response |
| topic | mollusk scallop-Vibrio interaction invertebrate immunity immune front-loading resistance to diseases |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1150280/full |
| work_keys_str_mv | AT eduardojeria resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT danieloyanedel resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT rodrigorojas resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT rodolfofarlora resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT rodolfofarlora resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT germanlira resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT anamercado resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT katherinemunoz resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT delphinedestoumieuxgarzon resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT katherinabrokordt resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse AT paulinaschmitt resistanceofargopectenpurpuratusscalloplarvaetovibriosisisassociatedwiththefrontloadingofimmunegenesandenhancedantimicrobialresponse |