Navigation within host tissues: Schistosoma mansoni and Trichobilharzia ocellata schistosomula respond to chemical gradients

Abstract

After penetration of human or duck host's skin schistosomula of Schistosoma mansoni and Trichobilharzia ocellata migrate parallel to the surface in the epidermis, then they enter the dermis and venules prior to further migration. This study focuses on potential behavioural mechanisms and host cues which may enable this navigation within host tissues. We stimulated cercariae to penetrate into agar substrates and to transform to schistosomula, and analysed their orientation behaviour within chemical concentration gradients. Both species were chemotactically attracted by low molecular weight fractions of their host's serum (human, duck) and d-glucose and l-arginine were identified as attractive components in serum. They responded to gradients, which established after addition of very low concentrations of d-glucose (1 μM in T. ocellata and 2 μM in S. mansoni) and l-arginine (0.025 μM in T. ocellata and 1.0 μM in S. mansoni). The response to d-glucose was specific as other saccharides had no stimulatory activity. l-Arginine stimulated chemotactic orientation both when free and bound in peptides. However, the two species responded differently to the position of l-arginine within the peptide (terminal or subterminal), and only S. mansoni, not T. ocellata, responded to peptides occurring in serum and endothelial cells: fibronectin (1 μM), bradykinin (25 pM) and its fragment 1–5 (2.5 μM). Both species adjusted their body axis with the ventral side towards the higher concentrations of d-glucose and of l-arginine. We argue that the chemotactic orientation and the alignment of the body axis enable the parasites (i) to orientate towards deeper skin layers and avoid accidental perforation of the covering skin surface layers, (ii) to determine their position during their surface-parallel migration within the epidermis, (iii) to locate blood vessels.