The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions

Manipulative parasites are predicted to liberate molecules in their external environment acting as manipulation factors with biological functions implicated in their host's physiological and behavioural alterations. These manipulation factors are expected to be part of a complex mixture called the secretome. While the secretomes of various parasites have been described, there is very little data for a putative manipulative parasite.

Here, we used proteomics to characterize the secretome of a model cestode with a complex life cycle based on trophic transmission.

We studied Schistocephalus solidus during the life stage in which behavioural changes have been described in its obligatory intermediate fish host, the threespine stickleback (Gasterosteus aculeatus). We re-sequenced the genome of S. solidus using a combination of long and short reads to improve protein coding gene prediction and annotation for this parasite species. We then described the whole worm's proteome and its secretome during fish host infection, using LC-MS/MS.

A total of 2 290 proteins were detected in the proteome of S. solidus, with 30 proteins detected only in the secretome. We found that the secretome contained proteases, proteins with neural and immune functions, as well as proteins involved in cell communication. We also detected Receptor-type tyrosine-protein phosphatases, which were reported in other parasitic systems to be strong manipulation factors. The secretome also contained a Phospholipid scramblase that clustered phylogenetically with a stickleback Phospholipid scramblase, suggesting it could have the potential to interfere with the function of the scramblase in the host's brain. Finally, we detected 12 S. solidus-specific proteins in the secretome that may play important roles in host-parasite interactions.

Our results suggest that this parasite liberates molecules with putative host manipulation functions in the host and that many of them are species specific.