Horizontal Transfer of msp130 Genes and the Evolution of Metazoan Biocalcification.

Abstract

The formation of calcified skeletons is crucial for the development, physiology, and ecology of many marine metazoans. The evolutionary origins of the genetic toolkit required for biocalcification are widely debated. MSP130 proteins, originally identified through their expression specifically by sea urchin skeletal cells, have been hypothesized to have been acquired by metazoans from bacteria through horizontal gene transfer. Here, we provide support for a horizontal gene transfer-based origin of metazoan MSP130 proteins by conducting phylogenetic and in silico protein analyses utilizing high-quality genomes. We show that msp130 genes underwent duplications within almost all biocalcifying bilaterian phyla and identify highly conserved intron-exon junctions specific to bilaterian msp130 genes. The absence of MSP130 proteins in calcifying, nonbilaterian metazoans and other basal eukaryotes suggests that an ancestral msp130 gene underwent a horizontal gene transfer event that predates bilaterians, but not metazoans. We report striking structural similarities between bilaterian and bacterial MSP130 proteins, with each containing a seven-bladed, barrel-like motif that encompasses a choice-of-anchor domain, and identify highly conserved, predicted Ca2+-binding sites associated with the barrels. These findings point to a conserved, ancient function for MSP130 proteins in biocalcification and support the view that lateral transfer of bacterial genes supported the appearance of calcified animal skeletons.