Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA.
Biol Direct. 2011 Oct 5;6:50. doi: 10.1186/1745-6150-6-50.
Volutin granules appear to be universally distributed and are morphologically and chemically identical to acidocalcisomes, which are electron-dense granular organelles rich in calcium and phosphate, whose functions include storage of phosphorus and various metal ions, metabolism of polyphosphate, maintenance of intracellular pH, osmoregulation and calcium homeostasis. Prokaryotes are thought to differ from eukaryotes in that they lack membrane-bounded organelles. However, it has been demonstrated that as in acidocalcisomes, the calcium and polyphosphate-rich intracellular "volutin granules (polyphosphate bodies)" in two bacterial species, Agrobacterium tumefaciens, and Rhodospirillum rubrum, are membrane bound and that the vacuolar proton-translocating pyrophosphatases (V-H+PPases) are present in their surrounding membranes. Volutin granules and acidocalcisomes have been found in organisms as diverse as bacteria and humans.
Here, we show volutin granules also occur in Archaea and are, therefore, present in the three superkingdoms of life (Archaea, Bacteria and Eukarya). Molecular analyses of V-H+PPase pumps, which acidify the acidocalcisome lumen and are diagnostic proteins of the organelle, also reveal the presence of this enzyme in all three superkingdoms suggesting it is ancient and universal. Since V-H+PPase sequences contained limited phylogenetic signal to fully resolve the ancestral nodes of the tree, we investigated the divergence of protein domains in the V-H+PPase molecules. Using Protein family (Pfam) database, we found a domain in the protein, PF03030. The domain is shared by 31 species in Eukarya, 231 in Bacteria, and 17 in Archaea. The universal distribution of the V-H+PPase PF03030 domain, which is associated with the V-H+PPase function, suggests the domain and the enzyme were already present in the Last Universal Common Ancestor (LUCA).
The importance of the V-H+PPase function and the evolutionary dynamics of these domains support the early origin of the acidocalcisome organelle. In particular, the universality of volutin granules and presence of a functional V-H+PPase domain in the three superkingdoms of life reveals that the acidocalcisomes may have appeared earlier than the divergence of the superkingdoms. This result is remarkable and highlights the possibility that a high degree of cellular compartmentalization could already have been present in the LUCA.
液泡铁蛋白颗粒似乎普遍存在，在形态和化学上与嗜酸囊泡相同，嗜酸囊泡是富含钙和磷酸盐的电子致密颗粒细胞器，其功能包括储存磷和各种金属离子、多磷酸盐代谢、维持细胞内 pH 值、渗透调节和钙稳态。原核生物被认为与真核生物不同，因为它们缺乏膜结合的细胞器。然而，已经证明，与嗜酸囊泡一样，两种细菌，根瘤菌和红螺菌，的富含钙和多磷酸盐的细胞内“液泡铁蛋白颗粒（多磷酸盐体）”是膜结合的，并且在其周围膜中存在液泡质子转运焦磷酸酶（V-H+PPase）。液泡铁蛋白颗粒和嗜酸囊泡已在细菌和人类等各种生物中发现。
在这里，我们表明液泡铁蛋白颗粒也存在于古菌中，因此存在于生命的三个超级王国（古菌、细菌和真核生物）中。对酸化嗜酸囊泡腔的 V-H+PPase 泵的分子分析，以及该细胞器的诊断蛋白，也表明这种酶存在于所有三个超级王国中，表明它是古老而普遍的。由于 V-H+PPase 序列包含有限的系统发育信号，无法完全解决树的祖先节点，我们研究了 V-H+PPase 分子中蛋白质结构域的分歧。使用蛋白质家族（Pfam）数据库，我们在蛋白质中发现了一个 PF03030 结构域。该结构域在真核生物中有 31 种，细菌中有 231 种，古菌中有 17 种。V-H+PPase PF03030 结构域的普遍分布与 V-H+PPase 功能相关，表明该结构域和酶在最后普遍共同祖先（LUCA）中就已经存在。
V-H+PPase 功能的重要性和这些结构域的进化动态支持嗜酸囊泡细胞器的早期起源。特别是，液泡铁蛋白颗粒的普遍性和生命的三个超级王国中存在功能性 V-H+PPase 结构域，表明嗜酸囊泡可能出现在超级王国的分化之前。这一结果引人注目，突出了细胞区室化程度很高的可能性在 LUCA 中已经存在。
