Carbonic Anhydrases: An Ancient Tool in Calcareous Sponge Biomineralization

Abstract

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.

Enhanced sequestration of carbon dioxide into calcium carbonate using pressure and a carbonic anhydrase from alkaliphilic Coleofasciculus chthonoplastes

“…Using the desiccator method, Müller et al achieved 55. 22 and 84.28 kg CaCO3 /m 3 h for 3 and 10 WAU/mL of a F I G U R E 4 SEM images of the crystals formed during the experiments at 10 bar with a CaCl 2 concentration of 100 mM. Pictures on the top panel correspond the experience without CA.…”

“…The whole mechanism is not completely understood but the potential motivates recent research [ 20 , 21 ]. Organisms seem to control precipitation to calcite [ 22 ], vaterite [ 23 ] or aragonite [ 24 ] via CA.…”

The genome of the reef-building glass spongeAphrocallistes vastusprovides insights into silica biomineralization

“…While different clades of organisms might not share key genes for biomineralization, there are many functional similarities between different mineralization systems: an organic scaffold, typically with alternating polar or charged residues (such as the amino acids DS, in the pearl oyster [ 38 ]), and accessory enzymes to process the inorganic ions (such as removal of H 2 O by carbonic anhydrase). In fact, some key genes, such as carbonic anhydrases, appear to be homologous and broadly used for biomineralization [ 39 , 40 ]. Proteins functioning as scaffolds for biomineralization are united by having an amino acid compositional bias and many regions of intrinsic disorder, and often will not align with each other, nor will they be found by the BLAST algorithm due to their low complexity [ 41 ].…”

“…Queries were: for glassin, the Euplectella curvistellata partial glassin genes (NCBI accessions LC010923.1 through LC012028.1 [ 9 ]) were used as queries. For carbonic anhydrases, we built on the dataset from Voigt et al [ 39 ], which was also used as queries. For cathepsins and silicateins, we built on the dataset from Aguilar-Camacho & McCormack [ 104 ].…”

Calcareous sponges can synthesize their skeleton under short-term ocean acidification

“…The spicules of P. magna showed the same shape in the control and low-pH conditions, the same as in the skeleton of adult individuals 20 . This might suggest that the proteins involved in the synthesis of these spicules (see 21,22 ) are not affected by OA. However, these proteins might be affected by temperature, as deformed spicules have been observed in S. hastifera under high temperatures 14 .…”