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Complex hierarchical microstructures of Cambrian mollusk Pelagiella: insight into early biomineralization and evolution.

ABSTRACT: Shell microstructure and mineralogy of Pelagiella madianensis Zhou & Xiao, 1984, a globally distributed Cambrian micromollusk, are investigated based on abundant and extraordinarily well-preserved specimens from Xinji Formation, Longxian, Shaanxi, North China. Five types of aragonitic microstructures have been recognized. The lamello-fibrillar microstructure, previously known from Pelagiella, constructs the outermost shell layer, while the remaining four types are reported here for the first time in this genus. They include fibrous foliated, foliated aragonite, crossed foliated lamellar and isolated tablets. The animal constructs these five types of microstructures to build its shell in a complex hierarchical pattern with four orders: crystallite columns, laths, folia and lamellae. These findings demonstrate that the capability of building complex shell microstructures had already evolved by the Cambrian explosion. In addition, this work shows that early aragonitic shells were constructed with fibers, laths, folia and isolated tablets, indicating increased controls over biomineralization by the animal.

SUBMITTER: Li L

PROVIDER: S-EPMC5434049 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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Complex hierarchical microstructures of Cambrian mollusk Pelagiella: insight into early biomineralization and evolution.

Li Luoyang L Zhang Xingliang X Yun Hao H Li Guoxiang G

Scientific reports 20170516 1

Shell microstructure and mineralogy of Pelagiella madianensis Zhou & Xiao, 1984, a globally distributed Cambrian micromollusk, are investigated based on abundant and extraordinarily well-preserved specimens from Xinji Formation, Longxian, Shaanxi, North China. Five types of aragonitic microstructures have been recognized. The lamello-fibrillar microstructure, previously known from Pelagiella, constructs the outermost shell layer, while the remaining four types are reported here for the first tim ...[more]

PMID: 28512325

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Project description:BACKGROUND: Calcium carbonate biominerals form often complex and beautiful skeletal elements, including coral exoskeletons and mollusc shells. Although the ability to generate these carbonate structures was apparently gained independently during animal evolution, it sometimes involves the same gene families. One of the best-studied of these gene families comprises the ?- carbonic anhydrases (CAs), which catalyse the reversible transformation of CO2 to HCO3 - and fulfill many physiological functions. Among Porifera -the oldest animal phylum with the ability to produce skeletal elements- only the class of calcareous sponges can build calcitic spicules, which are the extracellular products of specialized cells, the sclerocytes. Little is known about the molecular mechanisms of their synthesis, but inhibition studies suggest an essential role of CAs. In order to gain insight into the evolution and function of CAs in biomineralization of a basal metazoan species, we determined the diversity and expression of CAs in the calcareous sponges Sycon ciliatum and Leucosolenia complicata by means of genomic screening, RNA-Seq and RNA in situ hybridization expression analysis. Active biomineralization was located with calcein-staining. RESULTS: We found that the CA repertoires of two calcareous sponge species are strikingly more complex than those of other sponges. By characterizing their expression patterns, we could link two CAs (one intracellular and one extracellular) to the process of calcite spicule formation in both studied species. The extracellular biomineralizing CAs seem to be of paralogous origin, a finding that advises caution against assuming functional conservation of biomineralizing genes based upon orthology assessment alone. Additionally, calcareous sponges possess acatalytic CAs related to human CAs X and XI, suggesting an ancient origin of these proteins. Phylogenetic analyses including CAs from genomes of all non-bilaterian phyla suggest multiple gene losses and duplications and presence of several CAs in the last common ancestor of metazoans. CONCLUSIONS: We identified two key biomineralization enzymes from the CA-family in calcareous sponges and propose their possible interaction in spicule formation. The complex evolutionary history of the CA family is driven by frequent gene diversification and losses. These evolutionary patterns likely facilitated the numerous events of independent recruitment of CAs into biomineralization within Metazoa.

Project description:Molluscan shells are among the most fascinating research objects because of their diverse morphologies and textures. The formation of these delicate biomineralized structures is a matrix-mediated process. A question that arises is what are the essential components required to build these exoskeletons. In order to understand the molecular mechanisms of molluscan shell formation, it is crucial to identify organic macromolecules in different shells from diverse taxa. In the case of bivalves, however, taxon sampling in previous shell proteomics studies are focused predominantly on representatives of the class Pteriomorphia such as pearl oysters, edible oysters and mussels. In this study, we have characterized the shell organic matrix from the crocus clam, Tridacna crocea, (Heterodonta) using various biochemical techniques, including SDS-PAGE, FT-IR, monosaccharide analysis, and enzyme-linked lectin assay (ELLA). Furthermore, we have identified a number of shell matrix proteins (SMPs) using a comprehensive proteomics approach combined to RNA-seq. The biochemical studies confirmed the presence of proteins, polysaccharides, and sulfates in the T. crocea shell organic matrix. Proteomics analysis revealed that the majority of the T. crocea SMPs are novel and dissimilar to known SMPs identified from the other bivalve species. Meanwhile, the SMP repertoire of the crocus clam also includes proteins with conserved functional domains such as chitin-binding domain, VWA domain, and protease inhibitor domain. We also identified BMSP (Blue Mussel Shell Protein, originally reported from Mytilus), which is widely distributed among molluscan shell matrix proteins. Tridacna SMPs also include low-complexity regions (LCRs) that are absent in the other molluscan genomes, indicating that these genes may have evolved in specific lineage. These results highlight the diversity of the organic molecules - in particular proteins - that are essential for molluscan shell formation.

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Complex hierarchical microstructures of Cambrian mollusk Pelagiella: insight into early biomineralization and evolution.

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Complex hierarchical microstructures of Cambrian mollusk Pelagiella: insight into early biomineralization and evolution.

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