Interactions between the Parasite Philasterides dicentrarchi and the Immune System of the Turbot Scophthalmus maximus. A Transcriptomic Analysis

• Published in: Biology (Basel, Switzerland) Switzerland), 2020-10, Vol.9 (10), p.337
• Main Authors: Valle, Alejandra, Leiro, Jose Manuel, Pereiro, Patricia, Figueras, Antonio, Novoa, Beatriz, Dirks, Ron P.H, Lamas, Jesus
• Format: Article
• Language: English
• Subjects: ABC transporter; Animal genetics; Apoptosis; Aquariums; Arachidonate 15-lipoxygenase; Cell adhesion; Cell cycle; Cell surface; Chemokine receptors; Ciliata; Ciliates; Cytochrome; Diseases; Electron transport chain; Experimental infection; Experiments; Fc receptors; Flatfishes; Gene expression; Gene regulation; Genetic aspects; Genetic research; Genomics; Glycolysis; Health aspects; Immune response; Immune system; Immunological research; infection; Infections; Inflammation; Innate immunity; Interleukin 10; Leukocytes; Parasites; Pathogens; Peritoneum; Philasterides dicentrarchi; Physiological aspects; Prostaglandins; Scophthalmus maximus; Seawater; Signal transduction; Transcription; Transcriptomics; Tricarboxylic acid cycle; turbot; Virulence; Zoological research
• ISSN: 2079-7737; 2079-7737
• DOI: 10.3390/biology9100337

The present study analyses the interactions between Philasterides dicentrarchi (a ciliate parasite that causes high mortalities in cultured flatfish) and the peritoneal cells of the turbot Scophthalmus maximus during an experimental infection. The transcriptomic response was evaluated in the parasites and in the fish peritoneal cells, at 1, 2 and 4 h post-infection (hpi) in turbot injected intraperitoneally (ip) with 107 ciliates and at 12 and 48 hpi in turbot injected ip with 105 ciliates. Numerous genes were differentially expressed (DE) in P. dicentrarchi, relative to their expression in control ciliates (0 hpi): 407 (369 were up-regulated) at 1 hpi, 769 (415 were up-regulated) at 2 hpi and 507 (119 were up-regulated) at 4 hpi. Gene ontology (GO) analysis of the DE genes showed that the most representative categories of biological processes affected at 1, 2 and 4 hpi were biosynthetic processes, catabolic processes, biogenesis, proteolysis and transmembrane transport. Twelve genes of the ABC transporter family and eight genes of the leishmanolysin family were DE at 1, 2 and 4 hpi. Most of these genes were strongly up-regulated (UR), suggesting that they are involved in P. dicentrarchi infection. A third group of UR genes included several genes related to ribosome biogenesis, DNA transcription and RNA translation. However, expression of tubulins and tubulin associated proteins, such as kinesins or dyneins, which play key roles in ciliate division and movement, was down-regulated (DR). Similarly, genes that coded for lysosomal proteins or that participate in the cell cycle mitotic control, glycolysis, the Krebs cycle and/or in the electron transport chain were also DR. The transcriptomic analysis also revealed that in contrast to many parasites, which passively evade the host immune system, P. dicentrarchi strongly stimulated turbot peritoneal cells. Many genes related to inflammation were DE in peritoneal cells at 1, 2 and 4 hpi. However, the response was much lower at 12 hpi and almost disappeared completely at 48 hpi in fish that were able to kill P. dicentrarchi during the first few hpi. The genes that were DE at 1, 2 and 4 hpi were mainly related to the apoptotic process, the immune response, the Fc-epsilon receptor signalling pathway, the innate immune response, cell adhesion, cell surface receptors, the NF-kappaB signalling pathway and the MAPK cascade. Expression of toll-like receptors 2, 5 and 13 and of several components of NF-κB, MAPK and JAK/S