The Magellania venosa Biomineralizing Proteome: A Window into Brachiopod Shell Evolution

Abstract

Brachiopods are a lineage of invertebrates well known for the breadth and depth of their fossil record. Although the quality of this fossil record attracts the attention of paleontologists, geochemists, and paleoclimatologists, modern day brachiopods are also of interest to evolutionary biologists due to their potential to address a variety of questions ranging from developmental biology to biomineralization. The brachiopod shell is a composite material primarily composed of either calcite or calcium phosphate in close association with proteins and polysaccharides which give these composite structures their material properties. The information content of these biomolecules, sequestered within the shell during its construction, has the potential to inform hypotheses focused on describing how brachiopod shell formation evolved. Here, using high throughput proteomic approaches and next generation sequencing, we have surveyed and characterized the first shell-proteome and shell-forming transcriptome of any brachiopod, the South American Magellania venosa (Rhynchonelliformea: Terebratulida). We find that the seven most abundant proteins present in the shell are unique to M. venosa, but that these proteins display biochemical features found in other metazoan biomineralization proteins. We can also detect some M. venosa proteins that display significant sequence similarity to other metazoan biomineralization proteins, suggesting that some elements of the brachiopod shell-forming proteome are deeply evolutionarily conserved. We also employed a variety of preparation methods to isolate shell proteins and find that in comparison to the shells of other spiralian invertebrates (such as mollusks) the shell ultrastructure of M. venosa may explain the effects these preparation strategies have on our results.

Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads

“…This probably indicates loss of these genes in the phoronid lineage, although we cannot exclude the possibility of misannotation. To explore the origin of mineralized tissues in lophophorates, we compared biomineralization-related genes among phoronids and brachiopods, including the mantle transcriptome of the brachiopod Magellania venosa 54 . We found only five shell matrix protein genes that are shared by Phoronis, Lingula and Magellania (Supplementary Fig.…”

“…Notably, most of these genes can also be found in other metazoans with functions other than biomineralization. We failed to find brachiopod-specific shell matrix proteins in the Phoronis genome (Supplementary Table 36) 11,54 . Thus, our findings suggest that lineage-specific gene expansions, acquisition of novel genes and redeployment of extracellular matrix genes are involved in the evolution of lophophorate biomineralization.…”

Deep conservation of bivalve nacre proteins highlighted by shell matrix proteomics of the Unionoida Elliptio complanata and Villosa lienosa

“…Indeed, FAM20C is a kinase that phosphorylates the majority of the phosphoproteome in the extracellular matrices of bones and teeth, constituting a key player in vertebrate biomineralization processes [66]. Other recent investigations have revealed the presence of FAM20C-containing protein in the shell matrix of the giant limpet Lottia gigantea [48] and of the brachiopod Magellania venosa [58]. The presence of such a key protein, regulating the biomineralization formation of vertebrates in the shell matrices of molluscs and brachiopods reinforces the idea of a common molecular machinery, supporting the scenario of a conserved biomineralization toolkit between different metazoan lineages.…”

The Evolution of Brachiopoda

“…Other studies have identified major conflicts between molecular and morphological phylogenetic analyses of extant brachiopod species (Saito et al 2001, Bitner & Cohen 2015. Genomic (Stechmann & Schlegel 1999, Helfenbein et al 2001, Endo et al 2005, Adachi et al 2013, Luo et al 2015 and, more recently, proteomic (Immel et al 2015, Jackson et al 2015) studies, as well as studies of gene expression in brachiopod species, are now being tackled, with exciting, compelling results (Altenburger et al 2011, Passamaneck et al 2015. Establishing relationships between genetic variation, gene expression, and morphology is the next frontier in linking geological and biological approaches to the study of brachiopod evolution.…”

“…I suspect that as more genomic and combined morphological and molecular analyses (Wiens 2009, Giribet 2010, Reeder et al 2015 are conducted, past results that appeared to be in conflict will be better resolved. Phylogenomic studies (Kocot et al 2013, Nesnidal et al 2013, Jackson et al 2015, Lemer et al 2015, Luo et al 2015 will also help clarify these disagreements, and allow us to interpret results with greater confidence than is possible at this time.…”