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Acting locally - affecting globally: RNA sequencing of gilthead sea bream with a mild Sparicotyle chrysophrii infection reveals effects on apoptosis, immune and hypoxia related genes

Background: Monogenean flatworms are the main fish ectoparasites inflicting serious economic losses in aquaculture.The polyopisthocotyleanSparicotyle chrysophriiparasitizes the gills of gilthead sea bream (GSB, Sparus aurata)causinganaemia, lamellae fusion and sloughing of epithelial cells, with the consequent hypoxia, emaciation, lethargy andmortality. Currently no preventive or curative measures against this disease exist and therefore information on the host-parasite interaction is crucial to find mitigation solutions for sparicotylosis. The knowledge about gene regulation inmonogenean-host models mostly comes from freshwater monopysthocotyleans and almost nothing is known aboutpolyopisthocotyleans. The current study aims to decipher the host response at local (gills) and systemic (spleen, liver)levels in farmed GSB with a mild naturalS. chrysophriiinfection by transcriptomic analysis. Results: Using Illumina RNA sequencing and transcriptomic analysis, a total of 2581 differentially expressed transcriptswere identified in infected fish when compared to uninfected controls. Gill tissues in contact with the parasite (P gills)displayed regulation of fewer genes (700) than gill portions not in contact with the parasite (NP gills) (1235), most likelydue to a local silencing effect of the parasite. The systemic reaction in the spleen was much higher than that at theparasite attachment site (local) (1240), and higher than in liver (334). NP gills displayed a strong enrichment of genesmainly related to immune response and apoptosis. Processes such as apoptosis, inflammation and cell proliferationdominated gills, whereas inhibition of apoptosis, autophagy, platelet activation, signalling and aggregation, andinflammasome were observed in spleen. Proteasome markers were increased in all tissues, whereas hypoxia-relatedgenes were down-regulated in gills and spleen. Conclusions: Contrasting forces seem to be acting at local and systemic levels. The splenic down-regulation could bepart of a hypometabolic response, to counteract the hypoxia induced by the parasite damage to the gills and toconcentrate the energy on defence and repair responses. Alternatively, it can be also interpreted as the often observedaction of helminths to modify host immunity in its own interest. These results provide the first toolkit for future studiestowards understanding and management of this parasitosis.

Sparus aurata, Sparicotyle chrysophrii, Gills, Monogenea, Ectoparasites, Illumina RNA-seq, Transcriptomics, Apoptosis, Immune response

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