Uncovering iron regulation with species‐specific transcriptome patterns in Atlantic and coho salmon during a Caligus rogercresseyi infestation

Abstract

Salmon species cultured in Chile evidence different levels of susceptibility to the sea louse Caligus rogercresseyi. These differences have mainly been associated with specific immune responses. Moreover, iron regulation seems to be an important mechanism to confer immunity during the host infestation. This response called nutritional immunity has been described in bacterial infections, despite that no comprehensive studies involving in marine ectoparasites infestation have been reported. With this aim, we analysed the transcriptome profiles of Atlantic and coho salmon infected with C. rogercresseyi to evidence modulation of the iron metabolism as a proxy of nutritional immune responses. Whole transcriptome sequencing was performed in samples of skin and head kidney from Atlantic and coho salmon infected with sea lice. RNA-seq analyses revealed significant upregulation of transcripts in both salmon species at 7 and 14 dpi in skin and head kidney, respectively. However, iron regulation transcripts were differentially modulated, evidencing species-specific expression profiles. Genes related to heme degradation and iron transport such as hepcidin, transferrin and haptoglobin were primary upregulated in Atlantic salmon; meanwhile, in coho salmon, genes associated with heme biosynthesis were strongly transcribed. In summary, Atlantic salmon, which are more susceptible to infestation, presented molecular mechanisms to deplete cellular iron availability, suggesting putative mechanisms of nutritional immunity. In contrast, resistant coho salmon were less affected by sea lice, mainly activating pro-inflammatory mechanisms to cope with infestation.

Gene Expression Response to Sea Lice in Atlantic Salmon Skin: RNA Sequencing Comparison Between Resistant and Susceptible Animals

“…Finally, the gene hepcidin-1 is also correlated with sea lice counts in lice-attachment sites. Hepcidin is a regulator of iron metabolism, which as mentioned in the introduction has been associated with response to C. rogercresseyi ( Valenzuela-Muñoz et al, 2017 ).…”

“…For instance, comparative analyses of Atlantic and coho salmon parasitized with C. rogercresseyi showed that despite both showing up-regulation of pro-inflammatory genes, the response was highly specific, characterized in coho by an activation of the TH1 response ( Valenzuela-Muñoz et al, 2016 ). Another study linked iron sequestration and depletion mechanisms to the Atlantic salmon immune response to C. rogercresseyi ( Valenzuela-Muñoz et al, 2017 ).…”

The race between host and sea lice in the Chilean salmon farming: a genomic approach

“…From the transcriptome of Atlantic and Coho salmon infected with C. rogercresseyi , a high number of transcripts associated with iron modulation was observed from a GO enrichment analysis (Valenzuela‐Muñoz et al . ,). Furthermore, Atlantic salmon exhibit a high number of transcripts with functions including ion binding, ferric ion binding and ferrous ion binding, processes that were not observed in Coho salmon after infestation (Valenzuela‐Muñoz et al .…”

“…Furthermore, Atlantic salmon exhibit a high number of transcripts with functions including ion binding, ferric ion binding and ferrous ion binding, processes that were not observed in Coho salmon after infestation (Valenzuela‐Muñoz et al . ,). Moreover, RT‐qPCR analysis showed high expression levels of aminolevulinic acid synthase (ALAs) and coproporphyrinogenase , genes involved in the haem biosynthesis process.…”

“…Additionally, iron transport genes such as ferritin, transferrin and IRP were upregulated in Coho salmon skin at early infestation times, while in Atlantic salmon they were overexpressed at 14 dpi (Valenzuela‐Muñoz et al . ,). Also, differences in iron homeostasis genes were observed between Atlantic salmon infested with C. rogercresseyi and L. salmonis .…”