Transcriptomic Adjustments in a Freshwater Ectoparasite Reveal the Role of Molecular Plasticity for Parasite Host Shift

Abstract

A parasite's lifestyle is characterized by a critical dependency on its host for feeding, shelter and/or reproduction. The ability of parasites to exploit new host species can reduce the risk associated with host dependency. The number of host species that can be infected by parasites strongly affects their ecological and evolutionary dynamics along with their pathogenic effects on host communities. However, little is known about the processes and the pathways permitting parasites to successfully infect alternative host species, a process known as host shift. Here, we tested whether molecular plasticity changes in gene expression and in molecular pathways could favor host shift in parasites. Focusing on an invasive parasite, Tracheliastes polycolpus, infecting freshwater fish, we conducted a transcriptomic study to compare gene expression in parasites infecting their main host species and two alternative host species. We found 120 significant differentially expressed genes (DEGs) between parasites infecting the different host species. A total of 90% of the DEGs were identified between parasites using the main host species and those using the two alternative host species. Only a few significant DEGs (seven) were identified when comparing parasites from the two alternative host species. Molecular pathways enriched in DEGs and associated with the use of alternative host species were related to cellular machinery, energetic metabolism, muscle activity and oxidative stress. This study strongly suggests that molecular plasticity is an important mechanism sustaining the parasite's ability to infect alternative hosts.

Keywords: emerging parasites; gene expression; host shift; parasite specificity; plasticity; rapid adaptation.

Figure 1

Volcano plot showing the log transformed adjusted p-values (i.e., false discovery rate, FDR) and the log fold changes for the 12,357 protein-coding genes of T. polycolpus transcriptome for: (a) the comparison between parasites infecting dace and minnow, respectively, (b) the comparison between parasites infecting dace and gudgeon, respectively, and (c) the comparison between parasites infecting minnow and gudgeon, respectively. Black dots refer to non-significant differentially expressed genes at a FDR of 5%. Red dots refer to significant differentially expressed genes at a FDR of 5%. Green dots refer to significant differentially expressed genes at a FDR of 1%, and blue dots refer to significant differentially expressed genes at a FDR of 1‰.

Figure 2

Heat map synthetizing gene expression profiles (higher Z-score refers to higher expression) according to a clustering approach based on the different 84 differentially expressed genes found in parasites sampled on different host species (dace, minnow and gudgeon, respectively). Genes are displayed on the y-axis, while samples (parasites) are displayed on the x-axis. Each parasite sample is named by the name of host species from which it was sampled (five parasite samples per host species).

Figure 3

Top 40 of the gene ontologies (GOs) that were the most enriched in differentially expressed genes in the comparison between (a) parasites infecting minnow and dace and (b) parasites infecting gudgeon and dace. Blue GOs are enriched in genes that are under-expressed when comparing parasites sampled on alternative host parasites to those sampled on the principal host species. Red GOs are enriched in genes that are over-expressed when comparing parasites sampled on alternative host parasites to those sampled on the principal host species. The total number of genes involved in each GO is given in brackets.