Abstract
Collagens are often considered a metazoan hallmark, with the fibril-forming fibrillar collagens present from sponges to human. From evolutionary studies, three fibrillar collagen clades (named A, B, and C) have been defined and shown to be present in mammals, whereas the emergence of the A and B clades predates the protostome/deuterostome split. Moreover, several C clade fibrillar collagen chains are present in some invertebrate deuterostome genomes but not in protostomes whose genomes have been sequenced. The newly sequenced genomes of the choanoflagellate Monosiga brevicollis, the demosponge Amphimedon queenslandica, and the cnidarians Hydra magnipapillata (Hydra) and Nematostella vectensis (sea anemone) allow us to have a better understanding of the origin and evolution of fibrillar collagens. Analysis of these genomes suggests that an ancestral fibrillar collagen gene arose at the dawn of the Metazoa, before the divergence of sponge and eumetazoan lineages. The duplication events leading to the formation of the three fibrillar collagen clades (A, B, and C) occurred before the eumetazoan radiation. Interestingly, only the B clade fibrillar collagens preserved their characteristic modular structure from sponge to human. This observation is compatible with the suggested primordial function of type V/XI fibrillar collagens in the initiation of the formation of the collagen fibrils.
Highlights
Like all collagens, the fibrillar molecules are made of three ␣ chains, which can either be identical or result from a combination of two or three genetically distinct ␣ chains
We have studied the evolution of fibrillar collagens by taking advantage of the publicly available genome data from the sponge Amphimedon queenslandica and the sea anemone Nematostella vectensis
Demosponge and Cnidarian Fibrillar Collagen Diversity— Aiming to understand the early evolution of fibrillar collagens, we searched the genomes and ESTs of one demosponge and two cnidarians for genes possessing triple helix and C-propeptide sequences similar to Hydra and human fibrillar collagens. This survey led to the characterization of seven fibrillar collagen ␣ chains in the demosponge A. queenslandica, named Amq1␣ to Amq7␣, and eight fibrillar collagen ␣ chains in the sea anemone N. vectensis, named Nve1␣ to Nve8␣
Summary
Data Base Searching—Sequences from metazoan fibrillar collagen chains used in this study were obtained either from the European Bioinformatics Institute, from previous work on mosquito, honeybee, and ascidian collagens [17], or from blast searches in sponge and cnidarian genomes. Each read isolated by this approach and its mate were used to construct contigs by repeating several cycles of blast analysis and contig assembly This strategy permitted us to assemble five genomic contigs and to characterize seven distinct genes encoding fibrillar collagen chains (termed Amq1␣ to Amq7␣). For the recently completed genomes of the cnidarian N. vectensis and the sea urchin Strongylocentrotus purpuratus, Blast analysis was carried out using Nematostella (evodevo.bu.edu/stellabase/) and sea urchin servers This allowed us to identify eight fibrillar collagen genes in Nematostella (called Nve1␣ to Nve8␣) and the Strongylocentrotus ortholog of the Paracentrotus lividus COLP6␣ gene [17]. In the absence of a good outgroup, some trees were rooted using the midpoint rooting method and the retree editor from the PHYLIP package
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