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MBE Advance Access published online on August 31, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl100
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© The Author 2006. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org
Accepted August 14, 2006

Research Article

Insights into Early Extracellular Matrix Evolution: Spongin Short Chain Collagen-related Proteins are Homologous to Basement Membrane Type IV Collagens and Form a Novel Family Widely Distributed in Invertebrates

Abdel Aouacheria 1, Christophe Geourjon 2, Nushin Aghajari 2, Vincent Navratil 3, Gilbert Deléage 2, Claire Lethias 2, and Jean-Yves Exposito 2 *

1 Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Claude Bernard Lyon 1, 69622 Villeurbanne Cedex, France; present address: Apoptosis and Oncogenesis Laboratory, Institut de Biologie et Chimie des Protéines (IBCP), UMR CNRS 5086, Université Claude Bernard Lyon 1, IFR128 BioSciences Lyon-Gerland, 7, Passage du Vercors, 69367 Lyon cedex 07, France
2 Institut de Biologie et Chimie des Protéines (IBCP), UMR CNRS 5086, Université Claude Bernard Lyon 1, IFR128 BioSciences Lyon-Gerland, 7, Passage du Vercors, 69367 Lyon cedex 07, France
3 Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, Université Claude Bernard Lyon 1, 69622 Villeurbanne Cedex, France

* To whom correspondence should be addressed.
Jean-Yves Exposito, E-mail: jy.exposito{at}ibcp.fr


  Abstract

Collagens are thought to represent one of the most important molecular innovations in the metazoan line. Basement membrane type IV collagen is present in all Eumetazoa and was found in Homoscleromorpha, a sponge group with a well-organized epithelium, which may represent the first stage of tissue differentiation during animal evolution. In contrast, spongin seems to be a demosponge-specific collagenous protein, which can totally substitute an inorganic skeleton, such as in the well-known bath sponge. In the fresh-water sponge Ephydatia mulleri, we previously characterized a family of short chain collagens that are likely to be main components of spongins. Using a combination of sequence- and structure-based methods, we present evidence of remote homology between the carboxyl-terminal non-collagenous NC1 domain of spongin short chain collagens and type IV collagen. Unexpectedly, spongin short chain collagen-related proteins were retrieved in non-sponge animals, suggesting that a family related to spongin constitutes an evolutionary sister to the type IV collagen family. Formation of the ancestral NC1 domain and divergence of the spongin short chain collagen-related and type IV collagen families may have occurred before the parazoan-eumetazoan split, the earliest divergence among extant animal phyla. Molecular phylogenetics based on NC1 domain sequences suggest distinct evolutionary histories for spongin short chain collagen-related and type IV collagen families that include spongin short chain collagen-related gene loss in the ancestors of Ecdyzosoa and of vertebrates. The fact that a majority of invertebrates encodes spongin short chain collagen-related proteins raises the important question to the possible function of its members. Considering the importance of collagens for animal structure and substratum attachment, both families may have played crucial roles in animal diversification.

Keywords: Extracellular matrix; basement membrane; spongin; collagen; remote homology; metazoan evolution.
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