Single cell transcriptomics of Atlantic salmon (Salmo salar L.) liver reveals cellular heterogeneity and immunological responses to challenge by Aeromonas salmonicida
International audience The liver is a multitasking organ with essential functions for vertebrate health spanning metabolism and immunity. In contrast to mammals, our understanding of liver cellular heterogeneity and its role in regulating immunological status remains poorly defined in fishes. Addres...
Published in: | Frontiers in Immunology |
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Format: | Article in Journal/Newspaper |
Language: | English |
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Online Access: | https://hal.inrae.fr/hal-04011974 https://hal.inrae.fr/hal-04011974/document https://hal.inrae.fr/hal-04011974/file/2022_Taylor_Front_Immunol.pdf https://doi.org/10.3389/fimmu.2022.984799 |
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ftuniparissaclay:oai:HAL:hal-04011974v1 2024-09-15T17:56:18+00:00 Single cell transcriptomics of Atlantic salmon (Salmo salar L.) liver reveals cellular heterogeneity and immunological responses to challenge by Aeromonas salmonicida Taylor, Richard Ruiz Daniels, Rose Dobie, Ross Naseer, Shahmir Clark, Thomas Henderson, Neil Boudinot, Pierre Martin, Samuel A.M. Macqueen, Daniel University of Edinburgh (Edin.) University of Aberdeen Virologie et Immunologie Moléculaires (VIM (UR 0892)) Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) 2022-08-24 https://hal.inrae.fr/hal-04011974 https://hal.inrae.fr/hal-04011974/document https://hal.inrae.fr/hal-04011974/file/2022_Taylor_Front_Immunol.pdf https://doi.org/10.3389/fimmu.2022.984799 en eng HAL CCSD Frontiers info:eu-repo/semantics/altIdentifier/doi/10.3389/fimmu.2022.984799 info:eu-repo/semantics/altIdentifier/pmid/36091005 hal-04011974 https://hal.inrae.fr/hal-04011974 https://hal.inrae.fr/hal-04011974/document https://hal.inrae.fr/hal-04011974/file/2022_Taylor_Front_Immunol.pdf doi:10.3389/fimmu.2022.984799 PUBMED: 36091005 WOS: 000850813300001 http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess ISSN: 1664-3224 EISSN: 1664-3224 Frontiers in Immunology https://hal.inrae.fr/hal-04011974 Frontiers in Immunology, 2022, 13, pp.984799. ⟨10.3389/fimmu.2022.984799⟩ liver single cell transcriptomics bacterial infection salmonid fish immune-metabolism cross talk [SDV.IMM]Life Sciences [q-bio]/Immunology info:eu-repo/semantics/article Journal articles 2022 ftuniparissaclay https://doi.org/10.3389/fimmu.2022.984799 2024-08-30T01:48:51Z International audience The liver is a multitasking organ with essential functions for vertebrate health spanning metabolism and immunity. In contrast to mammals, our understanding of liver cellular heterogeneity and its role in regulating immunological status remains poorly defined in fishes. Addressing this knowledge gap, we generated a transcriptomic atlas of 47,432 nuclei isolated from the liver of Atlantic salmon ( Salmo salar L.) contrasting control fish with those challenged with a pathogenic strain of Aeromonas salmonicida , a problematic bacterial pathogen in global aquaculture. We identified the major liver cell types and their sub-populations, revealing poor conservation of many hepatic cell marker genes utilized in mammals, while identifying novel heterogeneity within the hepatocyte, lymphoid, and myeloid lineages. This included polyploid hepatocytes, multiple T cell populations including γδ T cells, and candidate populations of monocytes/macrophages and dendritic cells. A dominant hepatocyte population radically remodeled its transcriptome following infection to activate the acute phase response and other defense functions, while repressing routine functions such as metabolism. These defense-specialized hepatocytes showed strong activation of genes controlling protein synthesis and secretion, presumably to support the release of acute phase proteins into circulation. The infection response further involved up-regulation of numerous genes in an immune-cell specific manner, reflecting functions in pathogen recognition and killing, antigen presentation, phagocytosis, regulation of inflammation, B cell differentiation and T cell activation. Overall, this study greatly enhances our understanding of the multifaceted role played by liver immune and non-immune cells in host defense and metabolic remodeling following infection and provides many novel cell-specific marker genes to empower future studies of this organ in fishes. Article in Journal/Newspaper Atlantic salmon Salmo salar Archives ouvertes de Paris-Saclay Frontiers in Immunology 13 |
institution |
Open Polar |
collection |
Archives ouvertes de Paris-Saclay |
op_collection_id |
ftuniparissaclay |
language |
English |
topic |
liver single cell transcriptomics bacterial infection salmonid fish immune-metabolism cross talk [SDV.IMM]Life Sciences [q-bio]/Immunology |
spellingShingle |
liver single cell transcriptomics bacterial infection salmonid fish immune-metabolism cross talk [SDV.IMM]Life Sciences [q-bio]/Immunology Taylor, Richard Ruiz Daniels, Rose Dobie, Ross Naseer, Shahmir Clark, Thomas Henderson, Neil Boudinot, Pierre Martin, Samuel A.M. Macqueen, Daniel Single cell transcriptomics of Atlantic salmon (Salmo salar L.) liver reveals cellular heterogeneity and immunological responses to challenge by Aeromonas salmonicida |
topic_facet |
liver single cell transcriptomics bacterial infection salmonid fish immune-metabolism cross talk [SDV.IMM]Life Sciences [q-bio]/Immunology |
description |
International audience The liver is a multitasking organ with essential functions for vertebrate health spanning metabolism and immunity. In contrast to mammals, our understanding of liver cellular heterogeneity and its role in regulating immunological status remains poorly defined in fishes. Addressing this knowledge gap, we generated a transcriptomic atlas of 47,432 nuclei isolated from the liver of Atlantic salmon ( Salmo salar L.) contrasting control fish with those challenged with a pathogenic strain of Aeromonas salmonicida , a problematic bacterial pathogen in global aquaculture. We identified the major liver cell types and their sub-populations, revealing poor conservation of many hepatic cell marker genes utilized in mammals, while identifying novel heterogeneity within the hepatocyte, lymphoid, and myeloid lineages. This included polyploid hepatocytes, multiple T cell populations including γδ T cells, and candidate populations of monocytes/macrophages and dendritic cells. A dominant hepatocyte population radically remodeled its transcriptome following infection to activate the acute phase response and other defense functions, while repressing routine functions such as metabolism. These defense-specialized hepatocytes showed strong activation of genes controlling protein synthesis and secretion, presumably to support the release of acute phase proteins into circulation. The infection response further involved up-regulation of numerous genes in an immune-cell specific manner, reflecting functions in pathogen recognition and killing, antigen presentation, phagocytosis, regulation of inflammation, B cell differentiation and T cell activation. Overall, this study greatly enhances our understanding of the multifaceted role played by liver immune and non-immune cells in host defense and metabolic remodeling following infection and provides many novel cell-specific marker genes to empower future studies of this organ in fishes. |
author2 |
University of Edinburgh (Edin.) University of Aberdeen Virologie et Immunologie Moléculaires (VIM (UR 0892)) Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) |
format |
Article in Journal/Newspaper |
author |
Taylor, Richard Ruiz Daniels, Rose Dobie, Ross Naseer, Shahmir Clark, Thomas Henderson, Neil Boudinot, Pierre Martin, Samuel A.M. Macqueen, Daniel |
author_facet |
Taylor, Richard Ruiz Daniels, Rose Dobie, Ross Naseer, Shahmir Clark, Thomas Henderson, Neil Boudinot, Pierre Martin, Samuel A.M. Macqueen, Daniel |
author_sort |
Taylor, Richard |
title |
Single cell transcriptomics of Atlantic salmon (Salmo salar L.) liver reveals cellular heterogeneity and immunological responses to challenge by Aeromonas salmonicida |
title_short |
Single cell transcriptomics of Atlantic salmon (Salmo salar L.) liver reveals cellular heterogeneity and immunological responses to challenge by Aeromonas salmonicida |
title_full |
Single cell transcriptomics of Atlantic salmon (Salmo salar L.) liver reveals cellular heterogeneity and immunological responses to challenge by Aeromonas salmonicida |
title_fullStr |
Single cell transcriptomics of Atlantic salmon (Salmo salar L.) liver reveals cellular heterogeneity and immunological responses to challenge by Aeromonas salmonicida |
title_full_unstemmed |
Single cell transcriptomics of Atlantic salmon (Salmo salar L.) liver reveals cellular heterogeneity and immunological responses to challenge by Aeromonas salmonicida |
title_sort |
single cell transcriptomics of atlantic salmon (salmo salar l.) liver reveals cellular heterogeneity and immunological responses to challenge by aeromonas salmonicida |
publisher |
HAL CCSD |
publishDate |
2022 |
url |
https://hal.inrae.fr/hal-04011974 https://hal.inrae.fr/hal-04011974/document https://hal.inrae.fr/hal-04011974/file/2022_Taylor_Front_Immunol.pdf https://doi.org/10.3389/fimmu.2022.984799 |
genre |
Atlantic salmon Salmo salar |
genre_facet |
Atlantic salmon Salmo salar |
op_source |
ISSN: 1664-3224 EISSN: 1664-3224 Frontiers in Immunology https://hal.inrae.fr/hal-04011974 Frontiers in Immunology, 2022, 13, pp.984799. ⟨10.3389/fimmu.2022.984799⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.3389/fimmu.2022.984799 info:eu-repo/semantics/altIdentifier/pmid/36091005 hal-04011974 https://hal.inrae.fr/hal-04011974 https://hal.inrae.fr/hal-04011974/document https://hal.inrae.fr/hal-04011974/file/2022_Taylor_Front_Immunol.pdf doi:10.3389/fimmu.2022.984799 PUBMED: 36091005 WOS: 000850813300001 |
op_rights |
http://creativecommons.org/licenses/by/ info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.3389/fimmu.2022.984799 |
container_title |
Frontiers in Immunology |
container_volume |
13 |
_version_ |
1810432513260126208 |