Characterization of a fibrillar collagen gene in sponges reveals the early evolutionary appearance of two collagen gene families.

Abstract

We have characterized cDNA and genomic clones coding for a sponge collagen. The partial cDNA has an open reading frame encoding 547 amino acid residues. The conceptual translation product contains a probably incomplete triple-helical domain (307 amino acids) with one Gly-Xaa-YaaZaa imperfection in the otherwise perfect Gly-Xaa-Yaa repeats and a carboxyl propeptide (240 amino acids) that includes 7 cysteine residues. Amino acid sequence comparisons indicate that this sponge collagen is homologous to vertebrate and sea urchin fibrillar coliagens. Partial characterization of the corresponding gene reveals an intron-exon organization clearly related to the fibrillar collagen gene family. The exons coding for the triple-helical domain are 54 base pairs (bp) or multiples thereof, except for a 57-bp exon containing the Gly-Xaa-YaaZaa coding sequence and for two unusual exons of 126 and 18 bp, respectively. This latter 18-bp exon marks the end of the triple-helical domain, contrary to the other known ribriflar collagen genes that contain exons coding for the junction between the triple-helical domain and the carboxyl propeptide. Compared to other fibrillar collagen genes, the introns are remarkably small. Hybridization to blotted RNAs established that the gene transcript is 4.9 kilobases. Together with previous results that showed the existence of a nonfibrillar collagen in the same species, these data demonstrate that at least two collagen gene families are represented in the most primitive metazoa.Collagens are multidomain, interactive proteins that constitute the main extracellular component of all multicellular animals (1). So far, 13 different collagen types have been described in vertebrates, most of them forming polymeric structures or being closely associated with other collagenous polymers. Collagen molecules are made of three a chains, which may or may not be identical. They are characterized by the presence of triple-helical domains, which contain GlyXaa-Yaa repeats, that are essential for helix formation (2). More than 20 genes encode the different a chains. With the exception of the gene coding for type X collagen (3, 4), the described collagen coding genes have a complex exon-intron organization. Among them, the genes coding for the fibrilforming collagens (types I, II, III, V, and XI) have a homologous organization (5-8) with, in particular, triple-helix coding exons related to a 54-base-pair (bp) unit. These exons are believed to have evolved from an ancestral unit of 54 bp encoding six Gly-Xaa-Yaa repeats (9). The nonfibrillar collagen genes examined so far have more variable structures even though a few 54-bp exon units have been described (10-13).Very few data have been reported on the collagen gene organization in invertebrates. Variable exon sizes have been found in the nonfibrillar collagen genes, either in Drosophila melanogaster (14)(15)(16) or in Caenorhabditis elegans (17, 18), contrary to the multiple 54-bp motif described recently in a fibrillar collagen gene of the sea urchin Paracen...

Invertebrate Data Predict an Early Emergence of Vertebrate Fibrillar Collagen Clades and an Anti-incest Model

“…Emergence of Vertebrate Fibrillar Collagen Clades-During the last decades, several studies have suggested that some invertebrate fibrillar ␣ chains appear to be closely related to vertebrate minor collagens (14,29,30). The recently suggested model of Boot-Handford et al (12) was very surprising in our view, especially with regard to the appearance of the B and C clades in vertebrates or just before their emergence.…”

A receptor tyrosine kinase from choanoflagellates: Molecular insights into early animal evolution

“…However, the long evolutionary history separating animals from fungi and the profound differences in their cell biology suggest that genes important for animal evolution may have arisen after the divergence of the two lineages. Furthermore, the diversity of signaling and adhesion molecules in the most basal animals, sponges and cnidarians, indicates that some of these protein families may have arisen before the origin and diversification of Metazoa (4)(5)(6). A better picture of the evolution of early animal genomes will require the identification of phylogenetically and biologically appropriate species for comparison with animals.…”

The TrpA protein of Trichodesmium erythraeum IMS101 is a non-fibril-forming collagen and a component of the outer sheath

“…For example, the sequences Gly-X-Gly of Riftia, a hydrothermal vent tube worm, or Gly-X-Y-Z seen in sponges, have been shown not to affect molecular stability and fibrillar integrity in these proteins (Sicot et al, 1997;Exposito & Garrone, 1990). In the a-chain of Riftia, there is a single replacement of a glycine with an alanine in the regular Gly-X-Y repeat that should cause a disturbance in the triple helical rigidity.…”