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Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization

Enzymes of the α-carbonic anhydrase gene family (CAs) are essential for the deposition of calcium carbonate biominerals. In calcareous sponges (phylum Porifera, class Calcarea), specific CAs are involved in the formation of calcite spicules, a unique trait and synapomorphy of this class. However, de...

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Autores principales: Voigt, Oliver, Fradusco, Benedetta, Gut, Carolin, Kevrekidis, Charalampos, Vargas, Sergio, Wörheide, Gert
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8058475/
https://www.ncbi.nlm.nih.gov/pubmed/33897759
http://dx.doi.org/10.3389/fgene.2021.624533
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author Voigt, Oliver
Fradusco, Benedetta
Gut, Carolin
Kevrekidis, Charalampos
Vargas, Sergio
Wörheide, Gert
author_facet Voigt, Oliver
Fradusco, Benedetta
Gut, Carolin
Kevrekidis, Charalampos
Vargas, Sergio
Wörheide, Gert
author_sort Voigt, Oliver
collection PubMed
description Enzymes of the α-carbonic anhydrase gene family (CAs) are essential for the deposition of calcium carbonate biominerals. In calcareous sponges (phylum Porifera, class Calcarea), specific CAs are involved in the formation of calcite spicules, a unique trait and synapomorphy of this class. However, detailed studies on the CA repertoire of calcareous sponges exist for only two species of one of the two Calcarea subclasses, the Calcaronea. The CA repertoire of the second subclass, the Calcinea, has not been investigated so far, leaving a considerable gap in our knowledge about this gene family in Calcarea. Here, using transcriptomic analysis, phylogenetics, and in situ hybridization, we study the CA repertoire of four additional species of calcareous sponges, including three from the previously unsampled subclass Calcinea. Our data indicate that the last common ancestor of Calcarea had four ancestral CAs with defined subcellular localizations and functions (mitochondrial/cytosolic, membrane-bound, and secreted non-catalytic). The evolution of membrane-bound and secreted CAs involved gene duplications and losses, whereas mitochondrial/cytosolic and non-catalytic CAs are evidently orthologous genes. Mitochondrial/cytosolic CAs are biomineralization-specific genes recruited for biomineralization in the last common ancestor of calcareous sponges. The spatial–temporal expression of these CAs differs between species, which may reflect differences between subclasses or be related to the secondary thickening of spicules during biomineralization that does not occur in all species. With this study, we extend the understanding of the role and the evolution of a key biomineralization gene in calcareous sponges.
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spelling pubmed-80584752021-04-22 Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization Voigt, Oliver Fradusco, Benedetta Gut, Carolin Kevrekidis, Charalampos Vargas, Sergio Wörheide, Gert Front Genet Genetics Enzymes of the α-carbonic anhydrase gene family (CAs) are essential for the deposition of calcium carbonate biominerals. In calcareous sponges (phylum Porifera, class Calcarea), specific CAs are involved in the formation of calcite spicules, a unique trait and synapomorphy of this class. However, detailed studies on the CA repertoire of calcareous sponges exist for only two species of one of the two Calcarea subclasses, the Calcaronea. The CA repertoire of the second subclass, the Calcinea, has not been investigated so far, leaving a considerable gap in our knowledge about this gene family in Calcarea. Here, using transcriptomic analysis, phylogenetics, and in situ hybridization, we study the CA repertoire of four additional species of calcareous sponges, including three from the previously unsampled subclass Calcinea. Our data indicate that the last common ancestor of Calcarea had four ancestral CAs with defined subcellular localizations and functions (mitochondrial/cytosolic, membrane-bound, and secreted non-catalytic). The evolution of membrane-bound and secreted CAs involved gene duplications and losses, whereas mitochondrial/cytosolic and non-catalytic CAs are evidently orthologous genes. Mitochondrial/cytosolic CAs are biomineralization-specific genes recruited for biomineralization in the last common ancestor of calcareous sponges. The spatial–temporal expression of these CAs differs between species, which may reflect differences between subclasses or be related to the secondary thickening of spicules during biomineralization that does not occur in all species. With this study, we extend the understanding of the role and the evolution of a key biomineralization gene in calcareous sponges. Frontiers Media S.A. 2021-04-07 /pmc/articles/PMC8058475/ /pubmed/33897759 http://dx.doi.org/10.3389/fgene.2021.624533 Text en Copyright © 2021 Voigt, Fradusco, Gut, Kevrekidis, Vargas and Wörheide. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Genetics
Voigt, Oliver
Fradusco, Benedetta
Gut, Carolin
Kevrekidis, Charalampos
Vargas, Sergio
Wörheide, Gert
Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization
title Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization
title_full Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization
title_fullStr Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization
title_full_unstemmed Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization
title_short Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization
title_sort carbonic anhydrases: an ancient tool in calcareous sponge biomineralization
topic Genetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8058475/
https://www.ncbi.nlm.nih.gov/pubmed/33897759
http://dx.doi.org/10.3389/fgene.2021.624533
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