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Evolution of vacuolar proton pyrophosphatase domains and volutin granules: clues into the early evolutionary origin of the acidocalcisome.

Seufferheld MJ, Kim KM, Whitfield J, Valerio A, Caetano-Anollés G - Biol. Direct (2011)

Bottom Line: Using Protein family (Pfam) database, we found a domain in the protein, PF03030.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).This result is remarkable and highlights the possibility that a high degree of cellular compartmentalization could already have been present in the LUCA.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA. seufferh@illinois.edu

ABSTRACT

Background: 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.

Results: 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).

Conclusion: 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.

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Electron micrographs thin sections of Agrobacterium tumefaciens(a &b) and Methanosarcina acetivorans (c & d). In panel (a), the arrow shows the partially filled acidocalcisome of A. tumefaciens containing electron dense material. In panel (b), the arrow shows an empty A. tumefaciens acidocalcisome. In panel (c), the arrow shows the electron dense volutin granule of M. acetivorans. In panel (d), the arrows show empty, partially, and completely filled volutin granules of M. acetivorans.
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Figure 1: Electron micrographs thin sections of Agrobacterium tumefaciens(a &b) and Methanosarcina acetivorans (c & d). In panel (a), the arrow shows the partially filled acidocalcisome of A. tumefaciens containing electron dense material. In panel (b), the arrow shows an empty A. tumefaciens acidocalcisome. In panel (c), the arrow shows the electron dense volutin granule of M. acetivorans. In panel (d), the arrows show empty, partially, and completely filled volutin granules of M. acetivorans.

Mentions: Volutin-polyP bodies occur in organisms spanning an enormous range of phylogenetic complexity from Bacteria and Archaea to unicellular eukaryotes to algae to plants to insects to humans. Volutin/polyphosphate electron dense granules exhibit varied internal patterns suggestive of sponge-like electron-dense spheres, and when fixed they look as empty or partially empty vacuoles. The volutin granules shown in a number of microorganisms appear to be identical to acidocalcisomes of Agrobacterium and Rhodospirillum and eukaryotes. While it may come as a surprise that volutin electron-dense granule from different organisms bear close similarity to acidocalcisomes, now we know that acidocalcisomes are virtually identical in size, composition and morphology to volutin-polyP bodies found in a vast array of organisms, including Archaea. Although the volutin granules present in Methanosarcina have not been yet confirmed to be acidocalcisomes, they are morphologically and chemically similar to the acidocalcisomes of Agrobacterium and Rhodospirillum [9,10]. The volutin granules of Methanosarcina have the same chemical profile, morphological characteristics (sponge like-structure) and high levels of phosphorous compounds and calcium [35-37] than acidocalcisomes. In addition, some of the Agrobacterium acidocalcisomes (Figure 1, panels A and B) appear like partially or empty vacuoles due to the fixation/staining protocol that may promote the diffusion of the electron dense material out of the acidocalcisome. Remarkably, the same phenomenon is observed in the volutin granules of Methanosarcina (Figure 1, panels C and D).


Evolution of vacuolar proton pyrophosphatase domains and volutin granules: clues into the early evolutionary origin of the acidocalcisome.

Seufferheld MJ, Kim KM, Whitfield J, Valerio A, Caetano-Anollés G - Biol. Direct (2011)

Electron micrographs thin sections of Agrobacterium tumefaciens(a &b) and Methanosarcina acetivorans (c & d). In panel (a), the arrow shows the partially filled acidocalcisome of A. tumefaciens containing electron dense material. In panel (b), the arrow shows an empty A. tumefaciens acidocalcisome. In panel (c), the arrow shows the electron dense volutin granule of M. acetivorans. In panel (d), the arrows show empty, partially, and completely filled volutin granules of M. acetivorans.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3198990&req=5

Figure 1: Electron micrographs thin sections of Agrobacterium tumefaciens(a &b) and Methanosarcina acetivorans (c & d). In panel (a), the arrow shows the partially filled acidocalcisome of A. tumefaciens containing electron dense material. In panel (b), the arrow shows an empty A. tumefaciens acidocalcisome. In panel (c), the arrow shows the electron dense volutin granule of M. acetivorans. In panel (d), the arrows show empty, partially, and completely filled volutin granules of M. acetivorans.
Mentions: Volutin-polyP bodies occur in organisms spanning an enormous range of phylogenetic complexity from Bacteria and Archaea to unicellular eukaryotes to algae to plants to insects to humans. Volutin/polyphosphate electron dense granules exhibit varied internal patterns suggestive of sponge-like electron-dense spheres, and when fixed they look as empty or partially empty vacuoles. The volutin granules shown in a number of microorganisms appear to be identical to acidocalcisomes of Agrobacterium and Rhodospirillum and eukaryotes. While it may come as a surprise that volutin electron-dense granule from different organisms bear close similarity to acidocalcisomes, now we know that acidocalcisomes are virtually identical in size, composition and morphology to volutin-polyP bodies found in a vast array of organisms, including Archaea. Although the volutin granules present in Methanosarcina have not been yet confirmed to be acidocalcisomes, they are morphologically and chemically similar to the acidocalcisomes of Agrobacterium and Rhodospirillum [9,10]. The volutin granules of Methanosarcina have the same chemical profile, morphological characteristics (sponge like-structure) and high levels of phosphorous compounds and calcium [35-37] than acidocalcisomes. In addition, some of the Agrobacterium acidocalcisomes (Figure 1, panels A and B) appear like partially or empty vacuoles due to the fixation/staining protocol that may promote the diffusion of the electron dense material out of the acidocalcisome. Remarkably, the same phenomenon is observed in the volutin granules of Methanosarcina (Figure 1, panels C and D).

Bottom Line: Using Protein family (Pfam) database, we found a domain in the protein, PF03030.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).This result is remarkable and highlights the possibility that a high degree of cellular compartmentalization could already have been present in the LUCA.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Crop Sciences, University of Illinois at Urbana-Champaign, Urbana, IL, USA. seufferh@illinois.edu

ABSTRACT

Background: 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.

Results: 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).

Conclusion: 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.

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