Horizontal gene transfer contributed to the evolution of extracellular surface structures: the freshwater polyp Hydra is covered by a complex fibrous cuticle containing glycosaminoglycans and proteins of the PPOD and SWT (sweet tooth) families.

Angelika Böttger,Astrid Heim,Andreas Geissner,Charles N David,Kristian Pfaller,Sandra Münder,Brendan J Mcconkey,Michael W Hess,Hans-Joachim Gabius,Johannes Altstätter,Rainer Deutzmann,Willi Salvenmoser,Andrew C Doxey,Barbara Pauly

doi:10.1371/journal.pone.0052278

Abstract

The single-cell layered ectoderm of the fresh water polyp Hydra fulfills the function of an epidermis by protecting the animals from the surrounding medium. Its outer surface is covered by a fibrous structure termed the cuticle layer, with similarity to the extracellular surface coats of mammalian epithelia. In this paper we have identified molecular components of the cuticle. We show that its outermost layer contains glycoproteins and glycosaminoglycans and we have identified chondroitin and chondroitin-6-sulfate chains. In a search for proteins that could be involved in organising this structure we found PPOD proteins and several members of a protein family containing only SWT (sweet tooth) domains. Structural analyses indicate that PPODs consist of two tandem β-trefoil domains with similarity to carbohydrate-binding sites found in lectins. Experimental evidence confirmed that PPODs can bind sulfated glycans and are secreted into the cuticle layer from granules localized under the apical surface of the ectodermal epithelial cells. PPODs are taxon-specific proteins which appear to have entered the Hydra genome by horizontal gene transfer from bacteria. Their acquisition at the time Hydra evolved from a marine ancestor may have been critical for the transition to the freshwater environment.

Highlights

The freshwater polyp Hydra belongs to the phylum cnidaria and is a representative of one of the earliest pre-bilaterian metazoans
Samples prepared in this way show the cuticle as a homogeneous coat covering the whole ectodermal surface (Fig. 1A)
The Freshwater Polyp Hydra is Covered by a Cuticle The present study shows that Hydra polyps are covered by an extracellular cuticle with a complex layered structure consisting of several proteins and glycosaminoglycans

Summary

Introduction

The freshwater polyp Hydra belongs to the phylum cnidaria and is a representative of one of the earliest pre-bilaterian metazoans. It has a simple body plan with an oral-aboral axis including a hypostome surrounded by tentacles, a gastric region and a peduncle with a basal disk. The tissue consists of two epithelia, the ectoderm and the endoderm, which are separated by the mesoglea, an extracellular matrix containing collagen and laminin [1]. In early electronmicroscopic studies of Hydra tissue, Lentz described the ectodermal extracellular surface as a ‘‘thin layer of homogeneous material of low density covered by a thicker feltwork of finely granular, fibrillar or filamentous material’’ with a thickness of 0.5 mm. Based on its ultrastructural similarity with the extracellular surface coats of mammalian epithelia, which line the lumina of blood vessels, intestine, kidney glomerular vessels and other organs, this extracellular layer was later termed glycocalyx in cnidarian literature (see for example [3,4,5])

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