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Cited by 12Aquaculture disease management and microbiotaParasite Biology and Host InteractionsInvertebrate Immune Response Mechanisms

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Keratinocytes drive the epithelial hyperplasia key to sea lice resistance in coho salmon

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Salisbury, S. J., Daniels, R. Ruiz, Monaghan, S. J., Bron, J. E., Villamayor, P. R., Gervais, O., Fast, M. D., Sveen, L., Houston, R. D., Robinson, N., Robledo, D.·2024·BMC Biology
DOI 10.1186/s12915-024-01952-8PMC PMC11287951

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Abstract

Background: Salmonid species have followed markedly divergent evolutionary trajectories in their interactions with sea lice. While sea lice parasitism poses significant economic, environmental, and animal welfare challenges for Atlantic salmon ( Salmo salar ) aquaculture, coho salmon ( Oncorhynchus kisutch ) exhibit near-complete resistance to sea lice, achieved through a potent epithelial hyperplasia response leading to rapid louse detachment. The molecular mechanisms underlying these divergent responses to sea lice are unknown. Results: We characterized the cellular and molecular responses of Atlantic salmon and coho salmon to sea lice using single-nuclei RNA sequencing. Juvenile fish were exposed to copepodid sea lice ( Lepeophtheirus salmonis ), and lice-attached pelvic fin and skin samples were collected 12 h, 24 h, 36 h, 48 h, and 60 h after exposure, along with control samples. Comparative analysis of control and treatment samples revealed an immune and wound-healing response that was common to both species, but attenuated in Atlantic salmon, potentially reflecting greater sea louse immunomodulation. Our results revealed unique but complementary roles of three layers of keratinocytes in the epithelial hyperplasia response leading to rapid sea lice rejection in coho salmon. Our results suggest that basal keratinocytes direct the expansion and mobility of intermediate and, especially, superficial keratinocytes, which eventually encapsulate the parasite. Conclusions: Our results highlight the key role of keratinocytes in coho salmon’s sea lice resistance and the diverged biological response of the two salmonid host species when interacting with this parasite. This study has identified key pathways and candidate genes that could be manipulated using various biotechnological solutions to improve Atlantic salmon sea lice resistance.

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Figures

Fig. 1 Cell types detected in Atlantic (a–c) and coho (d–f) salmon. UMAPs of cell clusters coloured by putative identity for a Atlantic salmon and b coho salmon. Violin plots of marker genes for each cell cluster for c Atlantic salmon and d coho salmon. Counts of each cell type by sample for e Atlantic salmon and f coho salmon. Note there is no 12 h fin or 24 h fin sample for Atlantic salmon
Fig. 1 Cell types detected in Atlantic (a–c) and coho (d–f) salmon. UMAPs of cell clusters coloured by putative identity for a Atlantic salmon and b coho salmon. Violin plots of marker genes for each cell cluster for c Atlantic salmon and d coho salmon. Counts of each cell type by sample for e Atlantic salmon and f coho salmon. Note there is no 12 h fin or 24 h fin sample for Atlantic salmonCC BY · PubMed Central
Fig. 2 Cell clusters identified integrating both Atlantic salmon and coho salmon samples using 1:1 orthologous genes. a UMAP of cell clusters split by species, b violin plot of expression of a marker gene for each cluster. Violin plots visualize the expression of these same features in the species-specific datasets: c Atlantic salmon, d coho salmon. The Atlantic salmon and coho salmon ortholog ENSEMBL codes are noted to the right of each gene
Fig. 2 Cell clusters identified integrating both Atlantic salmon and coho salmon samples using 1:1 orthologous genes. a UMAP of cell clusters split by species, b violin plot of expression of a marker gene for each cluster. Violin plots visualize the expression of these same features in the species-specific datasets: c Atlantic salmon, d coho salmon. The Atlantic salmon and coho salmon ortholog ENSEMBL codes are noted to the right of each geneCC BY · PubMed Central
Fig. 3 Sub-clustering of putative immune cells expressing CD45. UMAP visualization of immune clusters in Atlantic (a) and coho (b) salmon. Dot plots of features characterizing immune cell types in Atlantic (c) and coho (d) salmon
Fig. 3 Sub-clustering of putative immune cells expressing CD45. UMAP visualization of immune clusters in Atlantic (a) and coho (b) salmon. Dot plots of features characterizing immune cell types in Atlantic (c) and coho (d) salmonCC BY · PubMed Central
Fig. 4 Dot plots of wound healing-related gene expression in Atlantic salmon and/or coho salmon in response to sea lice. All genes shown were significantly differentially expressed (padj < 0.001) in at least one pairwise comparison between the control and any treatment time point in either species
Fig. 4 Dot plots of wound healing-related gene expression in Atlantic salmon and/or coho salmon in response to sea lice. All genes shown were significantly differentially expressed (padj < 0.001) in at least one pairwise comparison between the control and any treatment time point in either speciesCC BY · PubMed Central
Fig. 5 Dot plots of immune-related gene expression in Atlantic salmon and/or coho salmon in response to sea lice. a Immune genes upregulated in both species, b MHC genes upregulated in both species, c complement immune system gene expression, d immune-related genes particularly upregulated in Atlantic salmon in response to sea lice. All genes shown were significantly differentially expressed (padj < 0.001) in at least one pairwise comparison between the control and any treatment time point in either species
Fig. 5 Dot plots of immune-related gene expression in Atlantic salmon and/or coho salmon in response to sea lice. a Immune genes upregulated in both species, b MHC genes upregulated in both species, c complement immune system gene expression, d immune-related genes particularly upregulated in Atlantic salmon in response to sea lice. All genes shown were significantly differentially expressed (padj < 0.001) in at least one pairwise comparison between the control and any treatment time point in either speciesCC BY · PubMed Central
Fig. 6 Red blood cell response to sea lice in Atlantic salmon and coho salmon. a Violin plots of gene expression in Atlantic salmon and coho salmon of genes significantly upregulated in coho salmon keratinocytes (padj < 0.001) in response to sea lice in at least one treatment time point relative to the control (*—padj < 0.001, **—padj < 0.0001, ***—padj < 0.00001), b significantly enriched biological GO terms (padj < 0.001) for red blood cells in response to sea lice in Atlantic salmon and coho salmon
Fig. 6 Red blood cell response to sea lice in Atlantic salmon and coho salmon. a Violin plots of gene expression in Atlantic salmon and coho salmon of genes significantly upregulated in coho salmon keratinocytes (padj < 0.001) in response to sea lice in at least one treatment time point relative to the control (*—padj < 0.001, **—padj < 0.0001, ***—padj < 0.00001), b significantly enriched biological GO terms (padj < 0.001) for red blood cells in response to sea lice in Atlantic salmon and coho salmonCC BY · PubMed Central
Fig. 7 Keratinocyte response to sea lice underlies coho salmon resistance to sea lice. a Dot plots of gene expression in Atlantic salmon and coho salmon of genes significantly upregulated in coho salmon keratinocytes (padj < 0.001) in response to sea lice in at least one treatment time point relative to the control, b proposed unique contributions of superficial, intermediate, and basal keratinocytes to epithelial hyperplasia immune response to sea lice in coho salmon, c significantly enriched biological GO terms (padj < 0.001) for superficial, intermediate, and basal keratinocytes in response to sea lice in Atlantic salmon and coho salmon. Differentially expressed genes in a and GO terms in c are colour-coded by the biological processes depicted in b that they are potentially associated with
Fig. 7 Keratinocyte response to sea lice underlies coho salmon resistance to sea lice. a Dot plots of gene expression in Atlantic salmon and coho salmon of genes significantly upregulated in coho salmon keratinocytes (padj < 0.001) in response to sea lice in at least one treatment time point relative to the control, b proposed unique contributions of superficial, intermediate, and basal keratinocytes to epithelial hyperplasia immune response to sea lice in coho salmon, c significantly enriched biological GO terms (padj < 0.001) for superficial, intermediate, and basal keratinocytes in response to sea lice in Atlantic salmon and coho salmon. Differentially expressed genes in a and GO terms in c are colour-coded by the biological processes depicted in b that they are potentially associated withCC BY · PubMed Central
Fig. 8 Violin plots of gene expression in Atlantic salmon and coho salmon in response to sea lice that are potentially regulating coho salmon’s epithelial hyperplasia response to sea lice. The cell type for which the expression of each gene is shown is noted to the right of each plot (*—padj < 0.001, **—padj < 0.0001, ***—padj < 0.00001.)
Fig. 8 Violin plots of gene expression in Atlantic salmon and coho salmon in response to sea lice that are potentially regulating coho salmon’s epithelial hyperplasia response to sea lice. The cell type for which the expression of each gene is shown is noted to the right of each plot (*—padj < 0.001, **—padj < 0.0001, ***—padj < 0.00001.)CC BY · PubMed Central

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Metadata

Authors
Salisbury, S. J., Daniels, R. R., Monaghan, S. J., Bron, J. E., Villamayor, P. R., Gervais, O., Fast, M. D., Sveen, L., Houston, R. D., Robinson, N., & Robledo, D.
Affiliations
  • Roslin Institute (GB)
  • University of Stirling (GB)
  • University of Prince Edward Island (CA)
  • Nofima (NO)
  • Deakin University (AU)
Corresponding author
  • Salisbury, S. J.
  • Robinson, N.
  • Robledo, D.
ORCID
Venue
BMC Biology
Publisher
Springer Science and Business Media LLC
Published
2024-07-29
Volume
22
Issue
1
Pages
160-160
ISSN
1741-7007 (ISSN-L)
DOI
10.1186/s12915-024-01952-8
PMC
PMC11287951
OpenAlex
W4401082749
Cited by
12
References
8
Citations by year
2026: 7 · 2025: 5
FWCI
1.99
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Stirling Online Research Repository (University of Stirling) (submittedVersion, cc-by)
  • IslandScholar (University of Prince Edward Island) (submittedVersion, cc-by)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
Funders
  • Fiskeri - og havbruksnæringens forskningsfond (901631)
  • Biotechnology and Biological Sciences Research Council (BB/V009818/1, BBS/E/D/20002172, BBS/E/D/30002275, BBS/E/D/10002070, BBS/E/RL/230002A, BB/V009990/1)
  • Natural Sciences and Engineering Research Council of Canada
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
  • Life Sciences › Immunology and Microbiology › Parasitology › Parasite Biology and Host Interactions
  • Life Sciences › Immunology and Microbiology › Immunology › Invertebrate Immune Response Mechanisms
Keywords
coho salmon, Atlantic salmon, Lepeophtheirus salmonis, epithelial hyperplasia, keratinocytes, host-parasite interactions, wound healing, immune response, single-nucleus RNA sequencing, salmonid aquaculture
MeSH terms
Animals, Fish Diseases, Host-Parasite Interactions, Hyperplasia, Keratinocytes, Oncorhynchus kisutch, Salmo salar, Copepoda, Disease Resistance

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