Unravelling turbot (Scophthalmus maximus) resistance to Aeromonas salmonicida: transcriptomic insights from two full-sibling families with divergent susceptibility

IntroductionFurunculosis, caused by the gram-negative bacterium Aeromonas salmonicida subsp. salmonicida, remains a significant threat to turbot (Scophthalmus maximus) aquaculture. Identifying genetic backgrounds with enhanced disease resistance is critical for improving aquaculture health managemen...

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Main Authors: Patricia Pereiro, Ricardo Tur, Miguel García, Antonio Figueras, Beatriz Novoa
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Immunology
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Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2024.1522666/full
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author Patricia Pereiro
Ricardo Tur
Miguel García
Antonio Figueras
Beatriz Novoa
author_facet Patricia Pereiro
Ricardo Tur
Miguel García
Antonio Figueras
Beatriz Novoa
author_sort Patricia Pereiro
collection DOAJ
description IntroductionFurunculosis, caused by the gram-negative bacterium Aeromonas salmonicida subsp. salmonicida, remains a significant threat to turbot (Scophthalmus maximus) aquaculture. Identifying genetic backgrounds with enhanced disease resistance is critical for improving aquaculture health management, reducing antibiotic dependency, and mitigating economic losses. MethodsIn this study, five full-sibling turbot families were challenged with A. salmonicida, which revealed one family with significantly greater resistance. Transcriptomic analyses (RNA-Seq) were performed on resistant and susceptible families, examining both naïve and 24-h postinfection (hpi) samples from head kidney and liver tissues. ResultsIn the absence of infection, differentially expressed genes (DEGs) were identified predominantly in the liver. Following infection, a marked increase in DEGs was observed in the head kidney, with many genes linked to immune functions. Interestingly, the resistant family displayed a more controlled inflammatory response and upregulation of genes related to antigen presentation and T-cell activity in the head kidney at early infection stages, which may have contributed to its increased survival rate. In the liver, transcriptomic differences between the families were associated mainly with cytoskeletal organization, cell cycle regulation, and metabolic processes, including insulin signalling and lipid metabolism, regardless of infection status. Additionally, many DEGs overlapped with previously identified quantitative trait loci (QTLs) associated with resistance to A. salmonicida, providing further insights into the genetic basis of disease resistance. DiscussionThis study represents the first RNA-Seq analysis comparing resistant and susceptible turbot families and contributes valuable knowledge for the development of selective breeding programs targeting disease resistance in turbot and other aquaculture species susceptible to A. salmonicida.
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spelling doaj-art-ae01210a48e0405193634c23be0bdebd2024-12-06T05:10:06ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-12-011510.3389/fimmu.2024.15226661522666Unravelling turbot (Scophthalmus maximus) resistance to Aeromonas salmonicida: transcriptomic insights from two full-sibling families with divergent susceptibilityPatricia Pereiro0Ricardo Tur1Miguel García2Antonio Figueras3Beatriz Novoa4Instituto de Investigaciones Marinas (IIM), Consejo Superior de Investigaciones Científicas (CSIC), Vigo, SpainNueva Pescanova Biomarine Center, S.L., O Grove, SpainNueva Pescanova Biomarine Center, S.L., O Grove, SpainInstituto de Investigaciones Marinas (IIM), Consejo Superior de Investigaciones Científicas (CSIC), Vigo, SpainInstituto de Investigaciones Marinas (IIM), Consejo Superior de Investigaciones Científicas (CSIC), Vigo, SpainIntroductionFurunculosis, caused by the gram-negative bacterium Aeromonas salmonicida subsp. salmonicida, remains a significant threat to turbot (Scophthalmus maximus) aquaculture. Identifying genetic backgrounds with enhanced disease resistance is critical for improving aquaculture health management, reducing antibiotic dependency, and mitigating economic losses. MethodsIn this study, five full-sibling turbot families were challenged with A. salmonicida, which revealed one family with significantly greater resistance. Transcriptomic analyses (RNA-Seq) were performed on resistant and susceptible families, examining both naïve and 24-h postinfection (hpi) samples from head kidney and liver tissues. ResultsIn the absence of infection, differentially expressed genes (DEGs) were identified predominantly in the liver. Following infection, a marked increase in DEGs was observed in the head kidney, with many genes linked to immune functions. Interestingly, the resistant family displayed a more controlled inflammatory response and upregulation of genes related to antigen presentation and T-cell activity in the head kidney at early infection stages, which may have contributed to its increased survival rate. In the liver, transcriptomic differences between the families were associated mainly with cytoskeletal organization, cell cycle regulation, and metabolic processes, including insulin signalling and lipid metabolism, regardless of infection status. Additionally, many DEGs overlapped with previously identified quantitative trait loci (QTLs) associated with resistance to A. salmonicida, providing further insights into the genetic basis of disease resistance. DiscussionThis study represents the first RNA-Seq analysis comparing resistant and susceptible turbot families and contributes valuable knowledge for the development of selective breeding programs targeting disease resistance in turbot and other aquaculture species susceptible to A. salmonicida.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1522666/fullturbot familiesAeromonas salmonicidafurunculosisdisease resistancetranscriptome sequencing
spellingShingle Patricia Pereiro
Ricardo Tur
Miguel García
Antonio Figueras
Beatriz Novoa
Unravelling turbot (Scophthalmus maximus) resistance to Aeromonas salmonicida: transcriptomic insights from two full-sibling families with divergent susceptibility
Frontiers in Immunology
turbot families
Aeromonas salmonicida
furunculosis
disease resistance
transcriptome sequencing
title Unravelling turbot (Scophthalmus maximus) resistance to Aeromonas salmonicida: transcriptomic insights from two full-sibling families with divergent susceptibility
title_full Unravelling turbot (Scophthalmus maximus) resistance to Aeromonas salmonicida: transcriptomic insights from two full-sibling families with divergent susceptibility
title_fullStr Unravelling turbot (Scophthalmus maximus) resistance to Aeromonas salmonicida: transcriptomic insights from two full-sibling families with divergent susceptibility
title_full_unstemmed Unravelling turbot (Scophthalmus maximus) resistance to Aeromonas salmonicida: transcriptomic insights from two full-sibling families with divergent susceptibility
title_short Unravelling turbot (Scophthalmus maximus) resistance to Aeromonas salmonicida: transcriptomic insights from two full-sibling families with divergent susceptibility
title_sort unravelling turbot scophthalmus maximus resistance to aeromonas salmonicida transcriptomic insights from two full sibling families with divergent susceptibility
topic turbot families
Aeromonas salmonicida
furunculosis
disease resistance
transcriptome sequencing
url https://www.frontiersin.org/articles/10.3389/fimmu.2024.1522666/full
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