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Three-dimensionally preserved soft tissues and calcareous hexactins in a Silurian sponge: implications for early sponge evolution.

ABSTRACT: Sponges (Porifera), as one of the earliest-branching animal phyla, are crucial for understanding early metazoan phylogeny. Recent studies of Lower Palaeozoic sponges have revealed a variety of character states and combinations unknown in extant taxa, challenging our views of early sponge morphology. The Herefordshire Konservat-Lagerstätte yields an abundant, diverse sponge fauna with three-dimensional preservation of spicules and soft tissue. Carduispongia pedicula gen. et sp. nov. possesses a single layer of hexactine spicules arranged in a regular orthogonal network. This spicule type and arrangement is characteristic of the reticulosans, which have traditionally been interpreted as early members of the extant siliceous Class Hexactinellida. However, the unusual preservation of the spicules of C. pedicula reveals an originally calcareous composition, which would be diagnostic of the living Class Calcarea. The soft tissue architecture closely resembles the complex sylleibid or leuconid structure seen in some modern calcareans and homoscleromorphs. This combination of features strongly supports a skeletal continuum between primitive calcareans and hexactinellid siliceans, indicating that the last common ancestor of Porifera was a spiculate, solitary, vasiform animal with a thin skeletal wall.

SUBMITTER: Nadhira A

PROVIDER: S-EPMC6689616 | biostudies-literature | 2019 Jul

REPOSITORIES: biostudies-literature

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Three-dimensionally preserved soft tissues and calcareous hexactins in a Silurian sponge: implications for early sponge evolution.

Nadhira Ardianty A Sutton Mark D MD Botting Joseph P JP Muir Lucy A LA Gueriau Pierre P King Andrew A Briggs Derek E G DEG Siveter David J DJ Siveter Derek J DJ

Royal Society open science 20190731 7

Sponges (Porifera), as one of the earliest-branching animal phyla, are crucial for understanding early metazoan phylogeny. Recent studies of Lower Palaeozoic sponges have revealed a variety of character states and combinations unknown in extant taxa, challenging our views of early sponge morphology. The Herefordshire Konservat-Lagerstätte yields an abundant, diverse sponge fauna with three-dimensional preservation of spicules and soft tissue. <i>Carduispongia pedicula</i> gen. et sp. nov. posses ...[more]

PMID: 31417767

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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.

Dataset Information

Three-dimensionally preserved soft tissues and calcareous hexactins in a Silurian sponge: implications for early sponge evolution.

Publications

Three-dimensionally preserved soft tissues and calcareous hexactins in a Silurian sponge: implications for early sponge evolution.

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