Abstract
The ability to construct a mineralized skeleton was a major innovation for the Metazoa during their evolution in the late Precambrian/early Cambrian. Porifera (sponges) hold an informative position for efforts aimed at unraveling the origins of this ability because they are widely regarded to be the earliest branching metazoans, and are among the first multi-cellular animals to display the ability to biomineralize in the fossil record. Very few biomineralization associated proteins have been identified in sponges so far, with no transcriptome or proteome scale surveys yet available. In order to understand what genetic repertoire may have been present in the last common ancestor of the Metazoa (LCAM), and that may have contributed to the evolution of the ability to biocalcify, we have studied the skeletal proteome of the coralline demosponge Vaceletia sp. and compare this to other metazoan biomineralizing proteomes. We bring some spatial resolution to this analysis by dividing Vaceletia’s aragonitic calcium carbonate skeleton into “head” and “stalk” regions. With our approach we were able to identify 40 proteins from both the head and stalk regions, with many of these sharing some similarity to previously identified gene products from other organisms. Among these proteins are known biomineralization compounds, such as carbonic anhydrase, spherulin, extracellular matrix proteins and very acidic proteins. This report provides the first proteome scale analysis of a calcified poriferan skeletal proteome, and its composition clearly demonstrates that the LCAM contributed several key enzymes and matrix proteins to its descendants that supported the metazoan ability to biocalcify. However, lineage specific evolution is also likely to have contributed significantly to the ability of disparate metazoan lineages to biocalcify.
Highlights
Biomineralization is a phenomenon that can be found throughout the tree of life
Available skeletal proteome datasets from metazoans such as molluscs [2,3,4,5], sea urchins [6, 7] and brachiopods [8,9,10] go some way towards addressing this issue, but to study the origins of metazoan biomineralization it is crucial to investigate the biomineralizing proteome of an early branching metazoan
After elimination of identifications not conforming to these criteria, and combining identifications apparently belonging to the same protein, we obtained a list of 122 accepted protein identifications (S1 Table: Vaceletia sp. skeleton matrix proteins)
Summary
Its appearance in the metazoan (animal) fossil record coincides with a rapid increase in their morphological diversity, suggesting that the evolution of this ability was one key factor that supported the Cambrian explosion (~540 mya). Much effort has been aimed at elucidating the genetic and molecular mechanisms that underlie the ability to biomineralize in disparate animal phyla. It has been proposed that the metazoan ability to build mineral skeletal elements evolved at least twenty times independently [1]. This estimate makes assumptions regarding the morphological homology of skeletal elements in disparate taxa, and assumes simplistic models of evolutionary gain/loss of mineralized elements while disregarding the underlying molecular mechanisms that fabricate these structures. Available skeletal proteome datasets from metazoans such as molluscs [2,3,4,5], sea urchins [6, 7] and brachiopods [8,9,10] go some way towards addressing this issue, but to study the origins of metazoan biomineralization it is crucial to investigate the biomineralizing proteome of an early branching metazoan
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