Transcriptome profiling of lumpfish (Cyclopterus lumpus) head kidney to Renibacterium salmoninarum at early and chronic infection stages

Dev Comp Immunol. 2024 Jul:156:105165. doi: 10.1016/j.dci.2024.105165. Epub 2024 Mar 16.

Abstract

Renibacterium salmoninarum causes Bacterial Kidney Disease (BKD) in several fish species. Atlantic lumpfish, a cleaner fish, is susceptible to R. salmoninarum. To profile the transcriptome response of lumpfish to R. salmoninarum at early and chronic infection stages, fish were intraperitoneally injected with either a high dose of R. salmoninarum (1 × 109 cells dose-1) or PBS (control). Head kidney tissue samples were collected at 28- and 98-days post-infection (dpi) for RNA sequencing. Transcriptomic profiling identified 1971 and 139 differentially expressed genes (DEGs) in infected compared with control samples at 28 and 98 dpi, respectively. At 28 dpi, R. salmoninarum-induced genes (n = 434) mainly involved in innate and adaptive immune response-related pathways, whereas R. salmoninarum-suppressed genes (n = 1537) were largely connected to amino acid metabolism and cellular processes. Cell-mediated immunity-related genes showed dysregulation at 98 dpi. Several immune-signalling pathways were dysregulated in response to R. salmoninarum, including apoptosis, alternative complement, JAK-STAT signalling, and MHC-I dependent pathways. In summary, R. salmoninarum causes immune suppression at early infection, whereas lumpfish induce a cell-mediated immune response at chronic infection. This study provides a complete depiction of diverse immune mechanisms dysregulated by R. salmoninarum in lumpfish and opens new avenues to develop immune prophylactic tools to prevent BKD.

Keywords: Bacterial kidney disease; Immune suppressive pathogen; Lumpfish; RNA sequencing; Renibacterium salmoninarum.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity / genetics
  • Animals
  • Chronic Disease
  • Fish Diseases* / immunology
  • Fish Diseases* / microbiology
  • Fish Proteins / genetics
  • Fish Proteins / metabolism
  • Fishes / immunology
  • Fishes / microbiology
  • Gene Expression Profiling*
  • Gram-Negative Bacterial Infections / immunology
  • Head Kidney* / immunology
  • Immunity, Innate* / genetics
  • Kidney Diseases / genetics
  • Kidney Diseases / immunology
  • Kidney Diseases / microbiology
  • Kidney Diseases / veterinary
  • Micrococcaceae / genetics
  • Micrococcaceae / immunology
  • Perciformes / immunology
  • Perciformes / microbiology
  • Renibacterium* / genetics
  • Renibacterium* / immunology
  • Transcriptome*

Substances

  • Fish Proteins

Supplementary concepts

  • Renibacterium salmoninarum