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Osmotically driven prey disintegration in the gastrovascular cavity of the green hydra by a pore-forming protein

Daniel Sher^*,1, Yelena Fishman^*, Naomi Melamed-Book, Mingliang Zhang^* and Eliahu Zlotkin^*,1

^* Department of Cell and Animal Biology

Confocal Microscopy Unit, Silberman Institute of Life Sciences, The Hebrew University, Jerusalem, Israel

¹Correspondence: Department of Cell and Animal Biology, Silberman Institute of Life Sciences, The Hebrew University, Jerusalem 91904, Israel. E-mail: dsher{at}pob.huji.ac.il or zlotkin{at}vms.huji.ac.il

Pore-forming proteins (PFPs) are water-soluble proteins able to integrate into target membranes to form transmembrane pores. They are common determinants of bacterial pathogenicity and are often found in animal venoms. We recently isolated and characterized Hydralysins (Hlns), paralytic PFPs from the venomous green hydra Chlorohydra viridissima that are not found within the nematocytes, suggesting they are not involved in prey capture. The present study aimed to decipher the biological role of Hlns. Using in situ hybridization and immunohistochemistry, we show that Hlns are expressed by digestive cells surrounding the gastrovascular cavity (GVC) of Chlorohydra and secreted onto the prey during feeding. At biologically relevant concentrations, Hlns bind prey membranes and form pores, lysing the cells and disintegrating the prey tissue. Hlns are unable to bind Chlorohydra membranes, thus protecting the producing animal from the destructive effect of its own cytolytic protein. We suggest that osmotic disintegration of the prey within the GVC by Hlns, followed by phagocytosis and intracellular digestion, allows the soft-bodied green hydra to feed on hard, cuticle-covered prey while lacking the physical means to mechanically disintegrate it. Our results extend the biological significance of PFPs beyond the commonly expected offensive or defensive roles.—Sher, D., Fishman, Y., Melamed-Book, N., Zhang, M., Zlotkin, E. Osmotically driven prey disintegration in the gastrovascular cavity of the green hydra by a pore-forming protein.

Key Words: chemical ecology • toxin • digestion • cnidaria