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.

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 e...

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Main Authors: Angelika Böttger, Andrew C Doxey, Michael W Hess, Kristian Pfaller, Willi Salvenmoser, Rainer Deutzmann, Andreas Geissner, Barbara Pauly, Johannes Altstätter, Sandra Münder, Astrid Heim, Hans-Joachim Gabius, Brendan J McConkey, Charles N David
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3531485?pdf=render
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spelling doaj-3beaa3f1a0eb46c399639e61109a9fed2020-11-25T02:47:27ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-01712e5227810.1371/journal.pone.0052278Horizontal 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 BöttgerAndrew C DoxeyMichael W HessKristian PfallerWilli SalvenmoserRainer DeutzmannAndreas GeissnerBarbara PaulyJohannes AltstätterSandra MünderAstrid HeimHans-Joachim GabiusBrendan J McConkeyCharles N DavidThe 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.http://europepmc.org/articles/PMC3531485?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Angelika Böttger
Andrew C Doxey
Michael W Hess
Kristian Pfaller
Willi Salvenmoser
Rainer Deutzmann
Andreas Geissner
Barbara Pauly
Johannes Altstätter
Sandra Münder
Astrid Heim
Hans-Joachim Gabius
Brendan J McConkey
Charles N David
spellingShingle Angelika Böttger
Andrew C Doxey
Michael W Hess
Kristian Pfaller
Willi Salvenmoser
Rainer Deutzmann
Andreas Geissner
Barbara Pauly
Johannes Altstätter
Sandra Münder
Astrid Heim
Hans-Joachim Gabius
Brendan J McConkey
Charles N David
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.
PLoS ONE
author_facet Angelika Böttger
Andrew C Doxey
Michael W Hess
Kristian Pfaller
Willi Salvenmoser
Rainer Deutzmann
Andreas Geissner
Barbara Pauly
Johannes Altstätter
Sandra Münder
Astrid Heim
Hans-Joachim Gabius
Brendan J McConkey
Charles N David
author_sort Angelika Böttger
title 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.
title_short 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.
title_full 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.
title_fullStr 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.
title_full_unstemmed 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.
title_sort 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.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2012-01-01
description 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.
url http://europepmc.org/articles/PMC3531485?pdf=render
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