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Transcriptome Profiling of Atlantic Salmon (Salmo salar) Parr With Higher and Lower Pathogen Loads Following Piscirickettsia salmonis Infection

Salmonid rickettsial septicemia (SRS), caused by Piscirickettsia salmonis, is one of the most devastating diseases of salmonids. However, the transcriptomic responses of Atlantic salmon (Salmon salar) in freshwater to an EM-90-like isolate have not been explored. Here, we infected Atlantic salmon pa...

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Autores principales: Xue, Xi, Caballero-Solares, Albert, Hall, Jennifer R., Umasuthan, Navaneethaiyer, Kumar, Surendra, Jakob, Eva, Skugor, Stanko, Hawes, Christopher, Santander, Javier, Taylor, Richard G., Rise, Matthew L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8758579/
https://www.ncbi.nlm.nih.gov/pubmed/35035387
http://dx.doi.org/10.3389/fimmu.2021.789465
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author Xue, Xi
Caballero-Solares, Albert
Hall, Jennifer R.
Umasuthan, Navaneethaiyer
Kumar, Surendra
Jakob, Eva
Skugor, Stanko
Hawes, Christopher
Santander, Javier
Taylor, Richard G.
Rise, Matthew L.
author_facet Xue, Xi
Caballero-Solares, Albert
Hall, Jennifer R.
Umasuthan, Navaneethaiyer
Kumar, Surendra
Jakob, Eva
Skugor, Stanko
Hawes, Christopher
Santander, Javier
Taylor, Richard G.
Rise, Matthew L.
author_sort Xue, Xi
collection PubMed
description Salmonid rickettsial septicemia (SRS), caused by Piscirickettsia salmonis, is one of the most devastating diseases of salmonids. However, the transcriptomic responses of Atlantic salmon (Salmon salar) in freshwater to an EM-90-like isolate have not been explored. Here, we infected Atlantic salmon parr with an EM-90-like isolate and conducted time-course qPCR analyses of pathogen load and four biomarkers (campb, hampa, il8a, tlr5a) of innate immunity on the head kidney samples. Transcript expression of three of these genes (except hampa), as well as pathogen level, peaked at 21 days post-injection (DPI). Multivariate analyses of infected individuals at 21 DPI revealed two infection phenotypes [lower (L-SRS) and higher (H-SRS) infection level]. Five fish from each group (Control, L-SRS, and H-SRS) were selected for transcriptome profiling using a 44K salmonid microarray platform. We identified 1,636 and 3,076 differentially expressed probes (DEPs) in the L-SRS and H-SRS groups compared with the control group, respectively (FDR = 1%). Gene ontology term enrichment analyses of SRS-responsive genes revealed the activation of a large number of innate (e.g. “phagocytosis”, “defense response to bacterium”, “inflammatory response”) and adaptive (e.g. “regulation of T cell activation”, “antigen processing and presentation of exogenous antigen”) immune processes, while a small number of general physiological processes (e.g. “apoptotic process”, development and metabolism relevant) was enriched. Transcriptome results were confirmed by qPCR analyses of 42 microarray-identified transcripts. Furthermore, the comparison of individuals with differing levels of infection (H-SRS vs. L-SRS) generated insights into the biological processes possibly involved in disease resistance or susceptibility. This study demonstrated a low mortality (~30%) EM-90-like infection model and broadened the current understanding of molecular pathways underlying P. salmonis-triggered responses of Atlantic salmon, identifying biomarkers that may assist to diagnose and combat this pathogen.
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spelling pubmed-87585792022-01-15 Transcriptome Profiling of Atlantic Salmon (Salmo salar) Parr With Higher and Lower Pathogen Loads Following Piscirickettsia salmonis Infection Xue, Xi Caballero-Solares, Albert Hall, Jennifer R. Umasuthan, Navaneethaiyer Kumar, Surendra Jakob, Eva Skugor, Stanko Hawes, Christopher Santander, Javier Taylor, Richard G. Rise, Matthew L. Front Immunol Immunology Salmonid rickettsial septicemia (SRS), caused by Piscirickettsia salmonis, is one of the most devastating diseases of salmonids. However, the transcriptomic responses of Atlantic salmon (Salmon salar) in freshwater to an EM-90-like isolate have not been explored. Here, we infected Atlantic salmon parr with an EM-90-like isolate and conducted time-course qPCR analyses of pathogen load and four biomarkers (campb, hampa, il8a, tlr5a) of innate immunity on the head kidney samples. Transcript expression of three of these genes (except hampa), as well as pathogen level, peaked at 21 days post-injection (DPI). Multivariate analyses of infected individuals at 21 DPI revealed two infection phenotypes [lower (L-SRS) and higher (H-SRS) infection level]. Five fish from each group (Control, L-SRS, and H-SRS) were selected for transcriptome profiling using a 44K salmonid microarray platform. We identified 1,636 and 3,076 differentially expressed probes (DEPs) in the L-SRS and H-SRS groups compared with the control group, respectively (FDR = 1%). Gene ontology term enrichment analyses of SRS-responsive genes revealed the activation of a large number of innate (e.g. “phagocytosis”, “defense response to bacterium”, “inflammatory response”) and adaptive (e.g. “regulation of T cell activation”, “antigen processing and presentation of exogenous antigen”) immune processes, while a small number of general physiological processes (e.g. “apoptotic process”, development and metabolism relevant) was enriched. Transcriptome results were confirmed by qPCR analyses of 42 microarray-identified transcripts. Furthermore, the comparison of individuals with differing levels of infection (H-SRS vs. L-SRS) generated insights into the biological processes possibly involved in disease resistance or susceptibility. This study demonstrated a low mortality (~30%) EM-90-like infection model and broadened the current understanding of molecular pathways underlying P. salmonis-triggered responses of Atlantic salmon, identifying biomarkers that may assist to diagnose and combat this pathogen. Frontiers Media S.A. 2021-12-31 /pmc/articles/PMC8758579/ /pubmed/35035387 http://dx.doi.org/10.3389/fimmu.2021.789465 Text en Copyright © 2021 Xue, Caballero-Solares, Hall, Umasuthan, Kumar, Jakob, Skugor, Hawes, Santander, Taylor and Rise https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Xue, Xi
Caballero-Solares, Albert
Hall, Jennifer R.
Umasuthan, Navaneethaiyer
Kumar, Surendra
Jakob, Eva
Skugor, Stanko
Hawes, Christopher
Santander, Javier
Taylor, Richard G.
Rise, Matthew L.
Transcriptome Profiling of Atlantic Salmon (Salmo salar) Parr With Higher and Lower Pathogen Loads Following Piscirickettsia salmonis Infection
title Transcriptome Profiling of Atlantic Salmon (Salmo salar) Parr With Higher and Lower Pathogen Loads Following Piscirickettsia salmonis Infection
title_full Transcriptome Profiling of Atlantic Salmon (Salmo salar) Parr With Higher and Lower Pathogen Loads Following Piscirickettsia salmonis Infection
title_fullStr Transcriptome Profiling of Atlantic Salmon (Salmo salar) Parr With Higher and Lower Pathogen Loads Following Piscirickettsia salmonis Infection
title_full_unstemmed Transcriptome Profiling of Atlantic Salmon (Salmo salar) Parr With Higher and Lower Pathogen Loads Following Piscirickettsia salmonis Infection
title_short Transcriptome Profiling of Atlantic Salmon (Salmo salar) Parr With Higher and Lower Pathogen Loads Following Piscirickettsia salmonis Infection
title_sort transcriptome profiling of atlantic salmon (salmo salar) parr with higher and lower pathogen loads following piscirickettsia salmonis infection
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8758579/
https://www.ncbi.nlm.nih.gov/pubmed/35035387
http://dx.doi.org/10.3389/fimmu.2021.789465
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