Transcriptome profiling of posterior kidney of brown trout, Salmo trutta, during proliferative kidney disease

Abstract

BackgroundTetracapsuloides bryosalmonae is a myxozoan parasite which causes economically important and emerging proliferative kidney disease (PKD) in salmonids. Brown trout, Salmo trutta is a native fish species of Europe, which acts as asymptomatic carriers for T. bryosalmonae. There is only limited information on the molecular mechanism involved in the kidney of brown trout during T. bryosalmonae development. We employed RNA sequencing (RNA-seq) to investigate the global transcriptome changes in the posterior kidney of brown trout during T. bryosalmonae development.MethodsBrown trout were exposed to the spores of T. bryosalmonae and posterior kidneys were collected from both exposed and unexposed control fish. cDNA libraries were prepared from the posterior kidney and sequenced. Bioinformatics analysis was performed using standard pipeline of quality control, reference mapping, differential expression analysis, gene ontology, and pathway analysis. Quantitative real time PCR was performed to validate the transcriptional regulation of differentially expressed genes, and their correlation with RNA-seq data was statistically analyzed.ResultsTranscriptome analysis identified 1169 differentially expressed genes in the posterior kidney of brown trout, out of which 864 genes (74%) were upregulated and 305 genes (26%) were downregulated. The upregulated genes were associated with the regulation of immune system process, vesicle-mediated transport, leucocyte activation, and transport, whereas the downregulated genes were associated with endopeptidase regulatory activity, phosphatidylcholine biosynthetic process, connective tissue development, and collagen catabolic process.ConclusionTo our knowledge, this is the first RNA-seq based transcriptome study performed in the posterior kidney of brown trout during active T. bryosalmonae development. Most of the upregulated genes were associated with the immune system process, whereas the downregulated genes were associated with other metabolic functions. The findings of this study provide insights on the immune responses mounted by the brown trout on the developing parasite, and the host molecular machineries modulated by the parasite for its successful multiplication and release.

Identification and Expression Profiling of Toll-Like Receptors of Brown Trout (Salmo trutta) during Proliferative Kidney Disease

“…The pathogen invasion activates TLRs that can mediate a cytokine response that induces an inflammatory reaction in the host tissues [76,77]. Similarly, differential expression of various cytokines and their receptors were observed in the posterior kidney of brown trout during active T. bryosalmonae proliferation [25]. In the present study, we could neither observe a clinical sign of the disease nor a gene regulation of all examined TLRs at the early (2 wpe) and late (17 wpe) phases of parasite infection in brown trout.…”

“…Moreover, transcriptome data serve as a valuable baseline resource to explore both host-parasite relationships [42]. Three TLRs (TLR1, TLR19, and TLR13-like) were differentially expressed in the kidney transcriptome of brown trout during active T. bryosalmonae sporogenesis [25]. The aim of this experiment was to gain insight about these TLRs and to investigate their expression patterns from an early phase (2 wpe) to late phase (17 wpe) of PKD in brown trout.…”

“…TLR1 and TLR19 had a single copy and were located on chromosome 3. Whereas, TLR13-like had multiple copies and the transcript of TLR13-like located in chromosome 1 (TLR13-like Chr1) had 99.76% identity with the input sequence [25]. Each TLR gene had a complete open reading frame ranging between 322 (TLR13-like Chr2) and 1027 (TLR13-like Chr1) amino acids.…”

“…PKD-infected rainbow trout exhibits high antibody response, the up-regulation of suppressors of cytokine signaling molecules, dysregulated B cell populations, and cytokines of T-helper cells [17][18][19][20][21][22][23]. Nevertheless, only a few experiments have been conducted in brown trout to understand the host immune responses [22,24,25], protein-protein interaction [26], and metabolic functions [27] during PKD pathogenesis.…”

“…In our recent transcriptome study, we identified three differentially expressed TLRs (TLR1, TLR19, and TLR13-like) in the kidney of brown trout during T. bryosalmonae development [25]. TLR1 is found in mammals belonging to the TLR1 subfamily, whereas TLR13 and TLR19 belong to the TLR11 subfamily [36].…”