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Interaction between the gilthead sea bream (Sparus aurata) and the gill-infecting monogenean Sparicotyle chrysophrii

Mediterranean aquaculture production of gilthead sea bream (GSB, Sparus aurata) is significantly affected by seasonal and recurrent outbreaks of the ectoparasite Sparicotyle chrysophrii. This polyopisthocotylean parasitizes the gill epithelium and feeds on fish blood. Infected fish display lethargy due to hypoxia and severe anaemia, and local histopathological changes encompass lamellar shortening, clubbing and synechiae, epithelial and chloride cell proliferation and fusion of the secondary lamellae. During the course of natural, mild chronic infections in fish farms, gilthead sea bream samples of spleen, liver, parasitized and nonparasitized gill portions, as well as Sparicotyle eggs, oncomiracidia and adults were taken. RNA-seq (Illumina HiSeq2500) was performed to compare tissue gene expression between control (non-infected) and infected fish. Host tissues libraries (n=32) with ~ 650 million singleend reads (20.5 million reads per sample, average) were mapped and annotated using the GSB draft genome (http://nutrigroup-iats.org/seabreamdb). In total, 2, 581 differentially expressed (DE) transcripts were identified (55.5% down-regulated and 45.5% up-regulated), of which 1, 710 (66.25%) were known protein-coding. The monogenean-sparid interaction was characterised by an exhaustive apoptotic response both in gill tissues in direct contact with the parasite attachment organ, and in those gill areas harbouring no parasites. Interestingly, all DE genes related to response to hypoxia were down-regulated in gill tissues and spleen. In gills, interferon-related transcripts were strongly up-regulated, whereas non-parasitized gill tissues showed up-regulation of genes involved in IL-10 signalling pathway. Spleen displayed a significant up-regulation of proliferation and activity of macrophages and lymphocytes, inferred from the up-regulation of genes involved in cell-cycle pathways and those required for MHC I, chemokines, immunoglobulins, and proteasome complexes, which supported a systemic response to the monogenean. These results are key to set solid bases to develop and test new strategies to prevent and mitigate this important disease in farmed fish.

monogenean Sparicotyle chrysophrii, sea bream Sparus aurata, RNA-seq, Th1/ Th2 response

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