The Teleost Thymus in Health and Disease: New Insights from Transcriptomic and Histopathological Analyses of Turbot, Scophthalmus maximus

Abstract

The thymus is a primary lymphoid organ that plays a pivotal role in the adaptive immune system. The immunobiology of the thymus in fish is considered to be similar to that of mammals, but it is actually poorly characterized in several cultured teleost species. In particular, while investigations in human and veterinary medicine have highlighted that the thymus can be affected by different pathological conditions, little is known about its response during disease in fish. To better understand the role of the thymus under physiological and pathological conditions, we conducted a study in turbot (Scophthalmus maximus), a commercially valuable flatfish species, combining transcriptomic and histopathological analyses. The myxozoan parasite Enteromyxum scophthalmi, which represents a major challenge to turbot production, was used as a model of infection. The thymus tissues of healthy fish showed overrepresented functions related to its immunological role in T-cell development and maturation. Large differences were observed between the transcriptomes of control and severely infected fish. Evidence of inflammatory response, apoptosis modulation, and declined thymic function associated with loss of cellularity was revealed by both genomic and morphopathological analyses. This study presents the first description of the turbot thymus transcriptome and provides novel insights into the role of this organ in teleosts’ immune responses.

Blood Transcriptomics of Turbot Scophthalmus maximus: A Tool for Health Monitoring and Disease Studies

“…Likewise, investigations on the kidney and spleen during enteromyxosis showed decreasing numbers of immunoreactive cells to IgM and down-regulation of immunoglobulin-related genes in heavily parasitized turbot [ 52 , 54 ]. The results of blood transcriptomics are then in accordance with those observations, indicating that humoral immunity is ineffective in turbot against enteromyxosis [ 16 , 19 ]. Further, the activation of the innate immunity reflected by the up-regulated genes of severely infected fish is consistent with the increase in the percentage of circulating granulocytes and of the respiratory burst previously reported [ 53 ].…”

“…This disease, which poses a serious threat to turbot aquaculture, is caused by the myxozoan parasite Enteromyxum scophthalmi [15], included in the EU H2020-funded project ParaFishControl as one of the most harmful parasitic species affecting the main European farmed teleosts (https://www.parafishcontrol.eu/, accessed on 16 April 2021). The transcriptomic profiles of the major lymphohematopoietic organs (kidney, spleen and thymus) and the main target organ (digestive tract) have been analyzed [15,16]. Nevertheless, the blood transcriptome has not been evaluated during enteromyxosis before, nor, to our knowledge, ever studied in this species.…”

Genome-wide identification of the MAPK gene family in turbot and its involvement in abiotic and biotic stress responses

“…In the SRA study of SRP308109, RNAseq was performed on blood in four levels of infected (incipient, slight, moderate, and severe) and not infected turbot (Ronza et al, 2021). In the SRA study of SRP255305, thymus tissues from control and infected turbot at 24 and 42 dpi were selected for RNA-seq (Ronza et al, 2020). In addition, five SRA studies were conducted under V. anguillarum challenge.…”

Genome-Wide Identification, Molecular Characterization, and Involvement in Response to Abiotic and Biotic Stresses of the HSP70 Gene Family in Turbot (Scophthalmus maximus)

“…Because of the essential functions of HSP70 genes in response to diverse stresses, systematically identifying and exploring their expression patterns under abiotic and biotic stresses is expected to be valuable for further functional studies and exhibit important practical significance in the development of efficient farming practices, thereby leading to an increase in turbot fitness in aquaculture production. Fortunately, high-quality genome assembly [ 33 ] and multiple published RNA-seq datasets resources [ 26 , 27 , 28 , 30 , 31 , 32 , 34 , 35 ] made available in recent years make it possible to perform systematic identification, phylogenetic analysis, and a functional study of HSP70 genes in the turbot.…”