Gene expression response to a nematode parasite in novel and native eel hosts

Invasive parasites are involved in population declines of new host species worldwide. The high susceptibilities observed in many novel hosts have been attributed to the lack of protective immunity to the parasites which native hosts acquired during their shared evolution. We experimentally infected Japanese eels (Anguilla japonica) and European eels (A. anguilla) with Anguillicola crassus, a nematode parasite that is native to the Japanese eel and invasive in the European eel. We inferred gene expression changes in head kidney tissue from both species, using RNA-seq data to determine the responses at two time points during the early stages of infection (3 and 23 days post-infection). At both time points, the novel host modified the expression of a larger and functionally more diverse set of genes than the native host. Strikingly, the native host regulated immune gene expression only at the earlier time point and to a small extent while the novel host regulated these genes at both time points. A low number of differentially expressed immune genes, especially in the native host, suggests that a systemic immune response was of minor importance during the early stages of infection. Transcript abundance of genes involved in cell respiration was reduced in the novel host which may affect its ability to cope with harsh conditions and energetically demanding activities. The observed gene expression changes in response to a novel parasite that we observed in a fish follow a general pattern observed in amphibians and mammals, and suggest that the disruption of physiological processes, rather than the absence of an immediate immune response, are responsible for the higher susceptibility of the novel host.Funding provided by: Senate Competition Committee of the Leibniz AssociationCrossref Funder Registry ID: Award Number: SAW-2014-SGN-3European eels and Japanese eels were experimentally infected with Anguillicola crassus larvae or sham-infected with PBS and sampled at 3 days post-infection or 23 days post-infection (n = 5 for each species, time point, and treatment). mRNA was paired-end sequenced on an Illumina HiSeq2500 or HiSeq4000 and reads were de novo assembled with Trinity. Raw reads and assemblies used to create the the count data are available from the BioProjects PRJNA419718 (European eel 3 dpi), PRJNA546508 (European eel 23 dpi & assembly), and PRJNA546510 (Japanese eel 3 & 23 dpi & assembly). Differentially expressed genes between infected and control eels were identified separately for species and time points using DESeq2 v.1.14.0 on read counts obtained with RSEM v.1.3.0 and a mean coverage cut-off >= 10. GO term enrichment analysis was done with GOstats v2.48.0 using custom background annotations obtained by blasting against UniProt/Swiss-Prot and searching the Pfam database integrated in Trinotate v3.2.0