A Grand Unified Theory of Biomineralization

The geological record indicates that the major animal phyla began biomineralizing in a relatively short interval of time during the Cambrian evolutionary explosion, about 525 Myr ago. Because these phyla diverged well before this biomineralization event, it was triggered either by an unprecedented lateral genetic transfer, or was the result of parallel exaptation of an ancestral biomineral system in many separate lineages. As magnetite (Fe 3 O 4) biomineralization is the most ancient matrix-mediated system, and is present in most animal groups, it may have served as this ancestral template for exaptation. Complete sequencing of the genome of a magnetotactic bacterium, and identifying the magnetite operon, might provide a 'road map' for unraveling the genetics of biomineralization in higher organisms, including humans. One of the most sobering things a modern biologist can do is to examine the results of a 2-D gel taken from biomineral-forming tissue. The complexity and the number of protein products involved in what looks like a rather simple biological process is daunting. Years of work can go into unraveling the identity and function of a single product, such as the sea-urchin SM50 protein [1]. Perhaps the despair is premature, as the existing complexity observed today had to evolve from a pre-existing, presumably simpler system. One major process by which complex biological systems evolve is by taking an existing genetic pattern that evolved for one function, and then duplicating it, linking it up differently, and adapting it for a new role. The nascent system is then gradually debugged and improved through the process of random mutation and natural selection. This evolutionary pattern has been termed 'exaptation' [2]. If the biomineralization systems present in the major animal phyla today evolved in this fashion, then it makes sense to examine that ancient system first, and to use it to provide an evolutionary road map for the modern processes. The paleontological record of biomineralization supports the idea that many animal groups experienced an evolutionary 'trigger' during the Cambrian Explosion, which, as noted below, is compatible with repeated exaptation of an ancestral processes. Certainly, there does seem to be some fundamental underlying immunological similarity between the macromolecules involved in hydroxyapatite formation in the vertebrates, and those involved in the aragonite present in molluscan nacre [3, 4]; freshly ground nacre fails to elicit an immune