Calcareous sponge genomes reveal complex evolution of α-carbonic anhydrases and two key biomineralization enzymes.

Calcareous sponge genomes reveal complex evolution of α-carbonic anhydrases and two key biomineralization enzymes.
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DOI:
10.1186/s12862-014-0230-z
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发表时间:
2014-11-25
影响因子:
3.4
通讯作者:
Adamska M
Adamska M
中科院分区:
生物学2区
文献类型:
--
作者:
Voigt O;Adamski M;Sluzek K;Adamska M

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碳酸钙生物矿物通常形成复杂而美丽的骨骼元素,包括珊瑚外骨骼和软体动物外壳。虽然这些碳酸盐结构的形成能力显然是在动物进化过程中独立获得的,但有时涉及相同的基因家族。这些基因家族中研究得最好的一个包括α-碳酸酐酶(CA),它催化CO2可逆转化为HCO 3 −,并实现许多生理功能。在多孔动物门-最古老的动物门与生产骨骼元素的能力-只有类钙质海绵可以建立钙化骨针,这是细胞外的产品专门的细胞,硬细胞。关于其合成的分子机制知之甚少,但抑制研究表明CA的重要作用。为了深入了解CA在基底后生动物生物矿化过程中的进化和功能,我们采用基因组筛选、RNA-Seq和RNA原位杂交表达分析等方法,研究了钙质海绵Sycon ciliatum和Leucosolenia complexata中CA的多样性和表达。钙黄绿素染色定位活性生物矿化。我们发现,CA剧目的两个钙质海绵物种是惊人的比其他海绵更复杂。通过表征它们的表达模式,我们可以将两个CA(一个细胞内和一个细胞外)与两个研究物种中方解石骨针形成的过程联系起来。细胞外生物矿化CA似乎是旁系同源的起源,这一发现建议谨慎假设生物矿化基因的功能保护仅基于直系评估。此外,钙质海绵具有与人类CA X和XI相关的催化CA,这表明这些蛋白质的古老起源。系统发育分析,包括CA从基因组的所有非两侧门建议多个基因的丢失和重复和存在的几个CA在最后的共同祖先的后生动物。我们确定了两个关键的生物矿化酶从CA家族在钙质海绵,并提出他们可能的相互作用骨针的形成。CA家族复杂的进化历史是由频繁的基因多样性和丢失驱动的。这些进化模式可能促进了许多事件的独立招聘CA到后生动物内的生物矿化。本文的在线版本(doi:10.1186/s12862-014-0230-z)包含补充材料,可供授权用户使用。
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 α- 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. 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. 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. The online version of this article (doi:10.1186/s12862-014-0230-z) contains supplementary material, which is available to authorized users.
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