Host–Parasite Interactions Revisited: Evidence of Horizontal Transfer of a Transposable Element Between a Snail and Its Parasite

In eukaryotes, horizontal gene transfer (HGT) often involves transposable elements (TEs), host-parasite relationships, aquatic environments, or any of them combined. Horizontal transfer of transposable elements is both impactful, owing to the subsequent transposition burst, and insightful, providing information on organisms' evolutionary history. The flatworm Schistosoma mansoni is a human parasite with two free-living aquatic stages (intercalated between a definitive human host and intermediate snail host) and has a sizable TE content. We aimed to identify and characterize potential instances of HGT leveraging new genomic resources available. Using the latest chromosome-scale genome assembly and available TE sequences for the S. mansoni genome, we identify that two TEs, named Perere-3 and Sr3, are putatively horizontally transferred. We demonstrate the presence of these TEs in the genomes of Schistosoma spp. intermediate hosts, most likely explained by HGT. Perere-3/Sr3 were also found across a wide range of additional organisms not susceptible to schistosome infection, including turtles, fish, and other mollusks. We propose that the patchy distribution of Perere-3/Sr3 across the phylogenetic tree is best explained by HGT. Our synonymous substitution calculations further support HGT, as divergence between schistosome and snail TE sequences is markedly lower than that observed for conserved orthologous genes. We propose that HGT is likely linked to schistosomes' parasitic nature as several snail species sharing the elements are susceptible to infection. However, the rationale for the presence of Perere-3/Sr3 in species beyond this relationship is unknown.