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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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Unrooted phylogram from Bayesian analysis of 279 V-H+PPase sequences from the three superkingdoms of life. Terminal branches of V-H+PPases are labeled with a solid square when the Pfam domain was found duplicated in the sequence. If the domain were found single, the terminal branch has no square. All the branches are labeled with the name of the species and accession number. Eukaryote species are represented with black letters, Bacteria with blue and Archaea with red.
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Figure 2: Unrooted phylogram from Bayesian analysis of 279 V-H+PPase sequences from the three superkingdoms of life. Terminal branches of V-H+PPases are labeled with a solid square when the Pfam domain was found duplicated in the sequence. If the domain were found single, the terminal branch has no square. All the branches are labeled with the name of the species and accession number. Eukaryote species are represented with black letters, Bacteria with blue and Archaea with red.

Mentions: The tree of V-H+PPase amino acid sequences is star-like and without much deep internal topological structure, suggesting the existence of limited phylogenetic signal in the sequence needed to dissect deeper phylogenetic relationships (Figure 2). It also suggests a relatively recent history of sequence diversification in the molecule. The eukaryal, bacterial and archaeal V-H+PPase sequences largely formed monophyletic groups and eukaryotic sequences mostly grouped according to established organismal classification, with unicellular eukaryotes being placed at the base of the clade and unicellular algae and plants diversifying later. However, there were several instances of sequences that group in a way contradictory to accepted classification. These atypical patterns could be explained by lateral gene transfer (LGT) events among Bacteria, Archaea and Eukarya, some of which may have occurred early in evolution. Alternatively, these unusual placements might simply be the result of phylogenetic error associated with using only a single gene for analysis [38].


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)

Unrooted phylogram from Bayesian analysis of 279 V-H+PPase sequences from the three superkingdoms of life. Terminal branches of V-H+PPases are labeled with a solid square when the Pfam domain was found duplicated in the sequence. If the domain were found single, the terminal branch has no square. All the branches are labeled with the name of the species and accession number. Eukaryote species are represented with black letters, Bacteria with blue and Archaea with red.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 2: Unrooted phylogram from Bayesian analysis of 279 V-H+PPase sequences from the three superkingdoms of life. Terminal branches of V-H+PPases are labeled with a solid square when the Pfam domain was found duplicated in the sequence. If the domain were found single, the terminal branch has no square. All the branches are labeled with the name of the species and accession number. Eukaryote species are represented with black letters, Bacteria with blue and Archaea with red.
Mentions: The tree of V-H+PPase amino acid sequences is star-like and without much deep internal topological structure, suggesting the existence of limited phylogenetic signal in the sequence needed to dissect deeper phylogenetic relationships (Figure 2). It also suggests a relatively recent history of sequence diversification in the molecule. The eukaryal, bacterial and archaeal V-H+PPase sequences largely formed monophyletic groups and eukaryotic sequences mostly grouped according to established organismal classification, with unicellular eukaryotes being placed at the base of the clade and unicellular algae and plants diversifying later. However, there were several instances of sequences that group in a way contradictory to accepted classification. These atypical patterns could be explained by lateral gene transfer (LGT) events among Bacteria, Archaea and Eukarya, some of which may have occurred early in evolution. Alternatively, these unusual placements might simply be the result of phylogenetic error associated with using only a single gene for analysis [38].

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.

Show MeSH