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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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Sequence conservation and transmembrane helical (TMH) make up of V-H+PPases. (A) Sequence conservation of the set of aligned V-H+PPase sequences illustrated with sequence conservation scores obtained with JALVIEW. (B) Pfam domain definitions and TMH regions in the V-H+PPase of R. rubrum. The plots show TMH definitions obtained with TMMOD and TOPCONS. TMMOD TMH definitions are given together with posterior probabilities of the existence of a TMH region. The TOPCONS definitions are from a consensus
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Figure 3: Sequence conservation and transmembrane helical (TMH) make up of V-H+PPases. (A) Sequence conservation of the set of aligned V-H+PPase sequences illustrated with sequence conservation scores obtained with JALVIEW. (B) Pfam domain definitions and TMH regions in the V-H+PPase of R. rubrum. The plots show TMH definitions obtained with TMMOD and TOPCONS. TMMOD TMH definitions are given together with posterior probabilities of the existence of a TMH region. The TOPCONS definitions are from a consensus

Mentions: An analysis of the mean distance between protein sequences using the JTT model with gaps excluded in the analysis showed that levels of sequence identity were 64.4%, much larger the 30% expected in the presence of high conservation levels. Using JALVIEW, we extracted conservation scores (in a scale from 0 to 11) for every nucleotide site with a proportion of gaps that is less than 25%. Analysis of the 523 sites (out of the total 1,652 in the alignment) that fulfills that criterion, shows the vast majority of sites have conservation scores above 7 (251 sites, 48%) and many have scores above 10 (90 sites, 17%) (Figure 3). These results support the notion that V-H+PPases have highly conserved protein sequences and that the variable regions have little or highly degraded phylogenetic signal. This explains the star-like appearance and poorly supported nature of the V-H+ PPase tree and suggests the V-H+PPase domain is old, and from a structural perspective, is highly canalized. This conclusion, together with its wide if not universal distribution in life, suggests that the most parsimonious explanation of the origin of this membrane-associated protein is in LUCA and not in any lineage of the diversified world of organisms, as the reviewer claims.


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)

Sequence conservation and transmembrane helical (TMH) make up of V-H+PPases. (A) Sequence conservation of the set of aligned V-H+PPase sequences illustrated with sequence conservation scores obtained with JALVIEW. (B) Pfam domain definitions and TMH regions in the V-H+PPase of R. rubrum. The plots show TMH definitions obtained with TMMOD and TOPCONS. TMMOD TMH definitions are given together with posterior probabilities of the existence of a TMH region. The TOPCONS definitions are from a consensus
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Sequence conservation and transmembrane helical (TMH) make up of V-H+PPases. (A) Sequence conservation of the set of aligned V-H+PPase sequences illustrated with sequence conservation scores obtained with JALVIEW. (B) Pfam domain definitions and TMH regions in the V-H+PPase of R. rubrum. The plots show TMH definitions obtained with TMMOD and TOPCONS. TMMOD TMH definitions are given together with posterior probabilities of the existence of a TMH region. The TOPCONS definitions are from a consensus
Mentions: An analysis of the mean distance between protein sequences using the JTT model with gaps excluded in the analysis showed that levels of sequence identity were 64.4%, much larger the 30% expected in the presence of high conservation levels. Using JALVIEW, we extracted conservation scores (in a scale from 0 to 11) for every nucleotide site with a proportion of gaps that is less than 25%. Analysis of the 523 sites (out of the total 1,652 in the alignment) that fulfills that criterion, shows the vast majority of sites have conservation scores above 7 (251 sites, 48%) and many have scores above 10 (90 sites, 17%) (Figure 3). These results support the notion that V-H+PPases have highly conserved protein sequences and that the variable regions have little or highly degraded phylogenetic signal. This explains the star-like appearance and poorly supported nature of the V-H+ PPase tree and suggests the V-H+PPase domain is old, and from a structural perspective, is highly canalized. This conclusion, together with its wide if not universal distribution in life, suggests that the most parsimonious explanation of the origin of this membrane-associated protein is in LUCA and not in any lineage of the diversified world of organisms, as the reviewer claims.

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