Understanding host response to infectious salmon anaemia virus in an Atlantic salmon cell line using single-cell RNA sequencing

Abstract Background Infectious Salmon Anaemia Virus (ISAV) is an Orthomixovirus that represents a large problem for salmonid aquaculture worldwide. Current prevention and treatment methods are only partially effective. Genetic selection and genome engineering have the potential to develop ISAV resis...

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Published in:BMC Genomics
Main Authors: Ophélie Gervais, Carolina Peñaloza, Remi Gratacap, Athina Papadopoulou, Mariana Beltrán, Neil C. Henderson, Ross D. Houston, Musa A. Hassan, Diego Robledo
Format: Article in Journal/Newspaper
Language:English
Published: BMC 2023
Subjects:
Online Access:https://doi.org/10.1186/s12864-023-09254-z
https://doaj.org/article/62c45d1b7b464617b3b43f74fba4ab43
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spelling ftdoajarticles:oai:doaj.org/article:62c45d1b7b464617b3b43f74fba4ab43 2023-05-15T15:30:42+02:00 Understanding host response to infectious salmon anaemia virus in an Atlantic salmon cell line using single-cell RNA sequencing Ophélie Gervais Carolina Peñaloza Remi Gratacap Athina Papadopoulou Mariana Beltrán Neil C. Henderson Ross D. Houston Musa A. Hassan Diego Robledo 2023-03-01T00:00:00Z https://doi.org/10.1186/s12864-023-09254-z https://doaj.org/article/62c45d1b7b464617b3b43f74fba4ab43 EN eng BMC https://doi.org/10.1186/s12864-023-09254-z https://doaj.org/toc/1471-2164 doi:10.1186/s12864-023-09254-z 1471-2164 https://doaj.org/article/62c45d1b7b464617b3b43f74fba4ab43 BMC Genomics, Vol 24, Iss 1, Pp 1-12 (2023) ISAV Salmo salar Single cell RNA-Seq Aquaculture SHK-1 Disease Biotechnology TP248.13-248.65 Genetics QH426-470 article 2023 ftdoajarticles https://doi.org/10.1186/s12864-023-09254-z 2023-04-09T00:35:34Z Abstract Background Infectious Salmon Anaemia Virus (ISAV) is an Orthomixovirus that represents a large problem for salmonid aquaculture worldwide. Current prevention and treatment methods are only partially effective. Genetic selection and genome engineering have the potential to develop ISAV resistant salmon stocks. Both strategies can benefit from an improved understanding of the genomic regulation of ISAV pathogenesis. Here, we used single-cell RNA sequencing of an Atlantic salmon cell line to provide the first high dimensional insight into the transcriptional landscape that underpins host-virus interaction during early ISAV infection. Results Salmon head kidney (SHK-1) cells were single-cell RNA sequenced at 24, 48 and 96 h post-ISAV challenge. At 24 h post infection, cells showed expression signatures consistent with viral entry, with genes such as PI3K, FAK or JNK being upregulated relative to uninfected cells. At 48 and 96 h, infected cells showed a clear anti-viral response, characterised by the expression of IFNA2 or IRF2. Uninfected bystander cells at 48 and 96 h also showed clear transcriptional differences, potentially suggesting paracrine signalling from infected cells. These bystander cells expressed pathways such as mRNA sensing, RNA degradation, ubiquitination or proteasome; and up-regulation of mitochondrial ribosome genes also seemed to play a role in the host response to the infection. Correlation between viral and host genes revealed novel genes potentially key for this fish-virus interaction. Conclusions This study has increased our understanding of the cellular response of Atlantic salmon during ISAV infection and revealed host-virus interactions at the cellular level. Our results highlight various potential key genes in this host-virus interaction, which can be manipulated in future functional studies to increase the resistance of Atlantic salmon to ISAV. Article in Journal/Newspaper Atlantic salmon Salmo salar Directory of Open Access Journals: DOAJ Articles BMC Genomics 24 1
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic ISAV
Salmo salar
Single cell RNA-Seq
Aquaculture
SHK-1
Disease
Biotechnology
TP248.13-248.65
Genetics
QH426-470
spellingShingle ISAV
Salmo salar
Single cell RNA-Seq
Aquaculture
SHK-1
Disease
Biotechnology
TP248.13-248.65
Genetics
QH426-470
Ophélie Gervais
Carolina Peñaloza
Remi Gratacap
Athina Papadopoulou
Mariana Beltrán
Neil C. Henderson
Ross D. Houston
Musa A. Hassan
Diego Robledo
Understanding host response to infectious salmon anaemia virus in an Atlantic salmon cell line using single-cell RNA sequencing
topic_facet ISAV
Salmo salar
Single cell RNA-Seq
Aquaculture
SHK-1
Disease
Biotechnology
TP248.13-248.65
Genetics
QH426-470
description Abstract Background Infectious Salmon Anaemia Virus (ISAV) is an Orthomixovirus that represents a large problem for salmonid aquaculture worldwide. Current prevention and treatment methods are only partially effective. Genetic selection and genome engineering have the potential to develop ISAV resistant salmon stocks. Both strategies can benefit from an improved understanding of the genomic regulation of ISAV pathogenesis. Here, we used single-cell RNA sequencing of an Atlantic salmon cell line to provide the first high dimensional insight into the transcriptional landscape that underpins host-virus interaction during early ISAV infection. Results Salmon head kidney (SHK-1) cells were single-cell RNA sequenced at 24, 48 and 96 h post-ISAV challenge. At 24 h post infection, cells showed expression signatures consistent with viral entry, with genes such as PI3K, FAK or JNK being upregulated relative to uninfected cells. At 48 and 96 h, infected cells showed a clear anti-viral response, characterised by the expression of IFNA2 or IRF2. Uninfected bystander cells at 48 and 96 h also showed clear transcriptional differences, potentially suggesting paracrine signalling from infected cells. These bystander cells expressed pathways such as mRNA sensing, RNA degradation, ubiquitination or proteasome; and up-regulation of mitochondrial ribosome genes also seemed to play a role in the host response to the infection. Correlation between viral and host genes revealed novel genes potentially key for this fish-virus interaction. Conclusions This study has increased our understanding of the cellular response of Atlantic salmon during ISAV infection and revealed host-virus interactions at the cellular level. Our results highlight various potential key genes in this host-virus interaction, which can be manipulated in future functional studies to increase the resistance of Atlantic salmon to ISAV.
format Article in Journal/Newspaper
author Ophélie Gervais
Carolina Peñaloza
Remi Gratacap
Athina Papadopoulou
Mariana Beltrán
Neil C. Henderson
Ross D. Houston
Musa A. Hassan
Diego Robledo
author_facet Ophélie Gervais
Carolina Peñaloza
Remi Gratacap
Athina Papadopoulou
Mariana Beltrán
Neil C. Henderson
Ross D. Houston
Musa A. Hassan
Diego Robledo
author_sort Ophélie Gervais
title Understanding host response to infectious salmon anaemia virus in an Atlantic salmon cell line using single-cell RNA sequencing
title_short Understanding host response to infectious salmon anaemia virus in an Atlantic salmon cell line using single-cell RNA sequencing
title_full Understanding host response to infectious salmon anaemia virus in an Atlantic salmon cell line using single-cell RNA sequencing
title_fullStr Understanding host response to infectious salmon anaemia virus in an Atlantic salmon cell line using single-cell RNA sequencing
title_full_unstemmed Understanding host response to infectious salmon anaemia virus in an Atlantic salmon cell line using single-cell RNA sequencing
title_sort understanding host response to infectious salmon anaemia virus in an atlantic salmon cell line using single-cell rna sequencing
publisher BMC
publishDate 2023
url https://doi.org/10.1186/s12864-023-09254-z
https://doaj.org/article/62c45d1b7b464617b3b43f74fba4ab43
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source BMC Genomics, Vol 24, Iss 1, Pp 1-12 (2023)
op_relation https://doi.org/10.1186/s12864-023-09254-z
https://doaj.org/toc/1471-2164
doi:10.1186/s12864-023-09254-z
1471-2164
https://doaj.org/article/62c45d1b7b464617b3b43f74fba4ab43
op_doi https://doi.org/10.1186/s12864-023-09254-z
container_title BMC Genomics
container_volume 24
container_issue 1
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