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Specific evolution of F1-like ATPases in mycoplasmas.

Béven L, Charenton C, Dautant A, Bouyssou G, Labroussaa F, Sköllermo A, Persson A, Blanchard A, Sirand-Pugnet P - PLoS ONE (2012)

Bottom Line: Phylogenomic studies identified two types of F(1)-like ATPase clusters, Type 2 and Type 3, characterized by a rapid evolution of sequences with the conservation of structural features.Proteomic analyses demonstrated that the seven encoded proteins were produced during growth in axenic media.Mutagenesis and complementation studies demonstrated an association of the Type 3 cluster with a major ATPase activity of membrane fractions.

View Article: PubMed Central - PubMed

Affiliation: University Bordeaux, UMR 1332 de Biologie du Fruit et Pathologie, Villenave d'Ornon, France.

ABSTRACT
F(1)F(0) ATPases have been identified in most bacteria, including mycoplasmas which have very small genomes associated with a host-dependent lifestyle. In addition to the typical operon of eight genes encoding genuine F(1)F(0) ATPase (Type 1), we identified related clusters of seven genes in many mycoplasma species. Four of the encoded proteins have predicted structures similar to the α, β, γ and ε subunits of F(1) ATPases and could form an F(1)-like ATPase. The other three proteins display no similarity to any other known proteins. Two of these proteins are probably located in the membrane, as they have three and twelve predicted transmembrane helices. Phylogenomic studies identified two types of F(1)-like ATPase clusters, Type 2 and Type 3, characterized by a rapid evolution of sequences with the conservation of structural features. Clusters encoding Type 2 and Type 3 ATPases were assumed to originate from the Hominis group of mycoplasmas. We suggest that Type 3 ATPase clusters may spread to other phylogenetic groups by horizontal gene transfer between mycoplasmas in the same host, based on phylogeny and genomic context. Functional analyses in the ruminant pathogen Mycoplasma mycoides subsp. mycoides showed that the Type 3 cluster genes were organized into an operon. Proteomic analyses demonstrated that the seven encoded proteins were produced during growth in axenic media. Mutagenesis and complementation studies demonstrated an association of the Type 3 cluster with a major ATPase activity of membrane fractions. Thus, despite their tendency toward genome reduction, mycoplasmas have evolved and exchanged specific F(1)-like ATPases with no known equivalent in other bacteria. We propose a model, in which the F(1)-like structure is associated with a hypothetical X(0) sector located in the membrane of mycoplasma cells.

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Model of an F1-likeX0 ATPase encoded by the seven-gene clusters of Types 2 and 3 specific to mycoplasmas.A. The F1-like complex model of Mmm was drawn by similarity with the crystal structure of the E. coli F1-ATPase (Pdb id: 3oaa) [27] with the help of the Pymol software (http://www.pymol.org) [28]. The X0 complex proteins of Mmm were schematized on the basis of 2D structure predictions. Proteins 1 and 5 are depicted associated with the membrane, in accordance with the predicted transmembrane segments. Based on in silico and experimental results, the F1-like complex, Protein 2 and the main part of Protein 5 were predicted to be cytoplasmic. Within this model, the F1-like and the X0 sectors are represented, but the way they could interact remains largely unclear. B. The genes of the clusters were arbitrarily numbered from 1 to 7. Gene names are indicated above the boxes representing the genes. TM, transmembrane segments. The proteins encoded by genes 3, 4, 6 and 7 were found to be related to the subunits γ, ε, α and β of the F1F0 ATPase, respectively.
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pone-0038793-g006: Model of an F1-likeX0 ATPase encoded by the seven-gene clusters of Types 2 and 3 specific to mycoplasmas.A. The F1-like complex model of Mmm was drawn by similarity with the crystal structure of the E. coli F1-ATPase (Pdb id: 3oaa) [27] with the help of the Pymol software (http://www.pymol.org) [28]. The X0 complex proteins of Mmm were schematized on the basis of 2D structure predictions. Proteins 1 and 5 are depicted associated with the membrane, in accordance with the predicted transmembrane segments. Based on in silico and experimental results, the F1-like complex, Protein 2 and the main part of Protein 5 were predicted to be cytoplasmic. Within this model, the F1-like and the X0 sectors are represented, but the way they could interact remains largely unclear. B. The genes of the clusters were arbitrarily numbered from 1 to 7. Gene names are indicated above the boxes representing the genes. TM, transmembrane segments. The proteins encoded by genes 3, 4, 6 and 7 were found to be related to the subunits γ, ε, α and β of the F1F0 ATPase, respectively.

Mentions: The Type 2 and Type 3 gene clusters did not display strong sequence similarity, but they were organized similarly and proteins encoded by genes 1, 2, 3 and 4 were of the similar lengths in the two types (Figures 6B and S2). We investigated the function of Type 2 and Type 3 clusters further, by analysing and comparing the predicted proteins. This analysis is illustrated in Figure S3 for proteins 1–7 from Mmm.


Specific evolution of F1-like ATPases in mycoplasmas.

Béven L, Charenton C, Dautant A, Bouyssou G, Labroussaa F, Sköllermo A, Persson A, Blanchard A, Sirand-Pugnet P - PLoS ONE (2012)

Model of an F1-likeX0 ATPase encoded by the seven-gene clusters of Types 2 and 3 specific to mycoplasmas.A. The F1-like complex model of Mmm was drawn by similarity with the crystal structure of the E. coli F1-ATPase (Pdb id: 3oaa) [27] with the help of the Pymol software (http://www.pymol.org) [28]. The X0 complex proteins of Mmm were schematized on the basis of 2D structure predictions. Proteins 1 and 5 are depicted associated with the membrane, in accordance with the predicted transmembrane segments. Based on in silico and experimental results, the F1-like complex, Protein 2 and the main part of Protein 5 were predicted to be cytoplasmic. Within this model, the F1-like and the X0 sectors are represented, but the way they could interact remains largely unclear. B. The genes of the clusters were arbitrarily numbered from 1 to 7. Gene names are indicated above the boxes representing the genes. TM, transmembrane segments. The proteins encoded by genes 3, 4, 6 and 7 were found to be related to the subunits γ, ε, α and β of the F1F0 ATPase, respectively.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3369863&req=5

pone-0038793-g006: Model of an F1-likeX0 ATPase encoded by the seven-gene clusters of Types 2 and 3 specific to mycoplasmas.A. The F1-like complex model of Mmm was drawn by similarity with the crystal structure of the E. coli F1-ATPase (Pdb id: 3oaa) [27] with the help of the Pymol software (http://www.pymol.org) [28]. The X0 complex proteins of Mmm were schematized on the basis of 2D structure predictions. Proteins 1 and 5 are depicted associated with the membrane, in accordance with the predicted transmembrane segments. Based on in silico and experimental results, the F1-like complex, Protein 2 and the main part of Protein 5 were predicted to be cytoplasmic. Within this model, the F1-like and the X0 sectors are represented, but the way they could interact remains largely unclear. B. The genes of the clusters were arbitrarily numbered from 1 to 7. Gene names are indicated above the boxes representing the genes. TM, transmembrane segments. The proteins encoded by genes 3, 4, 6 and 7 were found to be related to the subunits γ, ε, α and β of the F1F0 ATPase, respectively.
Mentions: The Type 2 and Type 3 gene clusters did not display strong sequence similarity, but they were organized similarly and proteins encoded by genes 1, 2, 3 and 4 were of the similar lengths in the two types (Figures 6B and S2). We investigated the function of Type 2 and Type 3 clusters further, by analysing and comparing the predicted proteins. This analysis is illustrated in Figure S3 for proteins 1–7 from Mmm.

Bottom Line: Phylogenomic studies identified two types of F(1)-like ATPase clusters, Type 2 and Type 3, characterized by a rapid evolution of sequences with the conservation of structural features.Proteomic analyses demonstrated that the seven encoded proteins were produced during growth in axenic media.Mutagenesis and complementation studies demonstrated an association of the Type 3 cluster with a major ATPase activity of membrane fractions.

View Article: PubMed Central - PubMed

Affiliation: University Bordeaux, UMR 1332 de Biologie du Fruit et Pathologie, Villenave d'Ornon, France.

ABSTRACT
F(1)F(0) ATPases have been identified in most bacteria, including mycoplasmas which have very small genomes associated with a host-dependent lifestyle. In addition to the typical operon of eight genes encoding genuine F(1)F(0) ATPase (Type 1), we identified related clusters of seven genes in many mycoplasma species. Four of the encoded proteins have predicted structures similar to the α, β, γ and ε subunits of F(1) ATPases and could form an F(1)-like ATPase. The other three proteins display no similarity to any other known proteins. Two of these proteins are probably located in the membrane, as they have three and twelve predicted transmembrane helices. Phylogenomic studies identified two types of F(1)-like ATPase clusters, Type 2 and Type 3, characterized by a rapid evolution of sequences with the conservation of structural features. Clusters encoding Type 2 and Type 3 ATPases were assumed to originate from the Hominis group of mycoplasmas. We suggest that Type 3 ATPase clusters may spread to other phylogenetic groups by horizontal gene transfer between mycoplasmas in the same host, based on phylogeny and genomic context. Functional analyses in the ruminant pathogen Mycoplasma mycoides subsp. mycoides showed that the Type 3 cluster genes were organized into an operon. Proteomic analyses demonstrated that the seven encoded proteins were produced during growth in axenic media. Mutagenesis and complementation studies demonstrated an association of the Type 3 cluster with a major ATPase activity of membrane fractions. Thus, despite their tendency toward genome reduction, mycoplasmas have evolved and exchanged specific F(1)-like ATPases with no known equivalent in other bacteria. We propose a model, in which the F(1)-like structure is associated with a hypothetical X(0) sector located in the membrane of mycoplasma cells.

Show MeSH
Related in: MedlinePlus