The evolution of metazoan α-carbonic anhydrases and their roles in calcium carbonate biomineralization

Abstract

The carbonic anhydrase (CA; EC 4.2.1.1) superfamily is a class of ubiquitous metallo-enzymes that catalyse the reversible hydration of carbon dioxide. The α-CA family, present in all metazoan clades, is a key enzyme involved in a wide range of physiological functions including pH regulation, respiration, photosynthesis, and biocalcification. This paper reviews the evolution of the α-CA family, with an emphasis on metazoan α-CA members involved in biocalcification. Phylogenetic analyses reveal a complex evolutionary history of α-CAs, and suggest α-CA was independently co-opted into a variety of skeleton forming roles (e.g. as a provider of HCO 3 − ions, a structural protein, a nucleation activator, etc.) in multiple metazoan lineages. This evolutionary history is most likely the result of multiple gene duplications coupled with the insertion of repetitive or non-repetitive low-complexity domains (RLCDs/LCDs). These domains, of largely unknown function, appear to be lineage-specific, and provide further support for the hypothesis of independent recruitment of α-CAs to diverse metazoan biocalcification processes. An analysis of α-CA sequences associated with biocalcification processes indicates that the domains involved in the activity and conformation of the active site are extremely conserved among metazoans.

Characterization of Carbonic Anhydrase 9 in the Alimentary Canal of Aedes aegypti and Its Relationship to Homologous Mosquito Carbonic Anhydrases

“…The spatially and temporally restricted expression of insect-specific CAs supports the hypothesis that insect CAs duplicated to take on diverse functions as specialized compartments evolved. Similar instances of CA specialization and gene duplication have been recorded in other more basal taxa [45]. AeCA9 is intertwined with a multitude of physiological processes, but the midgut is the region of focus of this manuscript.…”

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

“…Many skeletal matrix proteins belong to families that are not necessarily specific for biomineralization processes, suggesting that many proteins could have been coopted secondarily for calcification purposes. For example, although CA has been observed in various biomineralization models, comprising eggshell, echinoderm skeleton, mollusc shell or sponge spicules, it constitutes a broad and ubiquitous protein family presenting various members in all organisms, calcifying or not; their phylogenetic analysis shows a very complex evolutionary history, indicating that they could have been recruited several times, in the independent manners, in biomineralization structure within the different metazoan clades [61]. At the opposite of the CA example, MSP-130 represents a remarkable illustration of a conserved molecular function that may be strictly restricted to biocalcification, but present in distinct metazoan lineages.…”

Chalky versus foliated: a discriminant immunogold labelling of shell microstructures in the edible oyster Crassostrea gigas

“…Then, several 473 members, referred to as nacrein-like proteins, were identified in numerous molluscs and other 474 metazoans. Nacreins and nacrein-like proteins exhibit similar primary structure: they possess 475 a carbonic anhydrase (CA) domain, the function of which is to reversibly catalyse the 476 conversion of carbon dioxide into bicarbonate (Le Roy et al 2014). In addition, they exhibit a 477 supernumerary domain, which is, in the present case, of the aspartic acid-rich type.…”

“…In addition, they exhibit a 477 supernumerary domain, which is, in the present case, of the aspartic acid-rich type. Such a 478 domain is likely to be involved in mineral interaction (Le Roy et al 2014). Finally, our 479 proteomic analysis identified a third member, a cell death abnormality protein 1-like 480 belonging to a group of conserved proteins involved in cell apoptosis.…”