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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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Distribution and evolution of extra copies of atpA-like and atpD-like genes in mollicutes.A. The number of typical F1F0 ATPase operons and of extra copies of atpA-like/atpD-like pairs of genes are indicated for each species. * In M. gallisepticum, one of the two extra copies only contains a truncated atpD-like gene. The 16S rDNA phylogenetic tree was generated by the ML method; bootstrap values of more than 50% are indicated. Bacillus subtilis was chosen as an outgroup species. Phylogenetic groups are indicated: S, Spiroplasma; H, Hominis; P, Pneumoniae; AP, Acholeplasma/Phytoplasma. Mnemonic codes are indicated in brackets besides species names when useful. B. The amino acid sequences of the proteins encoded by the atpA-like and atpD-like genes were concatenated and a multiple alignment was generated. Protein sequences of Type 1 atpA and atpD genes from M. pulmonis and B. subtilis (GenBank ID: atpA, NP_391564.1; atpD, NP_391562.1) were used as outgroup. The multiple sequence alignment was curated with GBLOCK to remove unreliable sites and a final round of manual editing was performed with Jalview. Phylogenetic trees were generated by ML, NJ and MP methods. The tree represented was obtained by the ML method. The aLRT/Bootstrap values corresponding to these three methods are indicated on the branches, in the following order: ML/NJ/MP. Sequences are labelled by their mnemonics, see also Table S2 for details.
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pone-0038793-g002: Distribution and evolution of extra copies of atpA-like and atpD-like genes in mollicutes.A. The number of typical F1F0 ATPase operons and of extra copies of atpA-like/atpD-like pairs of genes are indicated for each species. * In M. gallisepticum, one of the two extra copies only contains a truncated atpD-like gene. The 16S rDNA phylogenetic tree was generated by the ML method; bootstrap values of more than 50% are indicated. Bacillus subtilis was chosen as an outgroup species. Phylogenetic groups are indicated: S, Spiroplasma; H, Hominis; P, Pneumoniae; AP, Acholeplasma/Phytoplasma. Mnemonic codes are indicated in brackets besides species names when useful. B. The amino acid sequences of the proteins encoded by the atpA-like and atpD-like genes were concatenated and a multiple alignment was generated. Protein sequences of Type 1 atpA and atpD genes from M. pulmonis and B. subtilis (GenBank ID: atpA, NP_391564.1; atpD, NP_391562.1) were used as outgroup. The multiple sequence alignment was curated with GBLOCK to remove unreliable sites and a final round of manual editing was performed with Jalview. Phylogenetic trees were generated by ML, NJ and MP methods. The tree represented was obtained by the ML method. The aLRT/Bootstrap values corresponding to these three methods are indicated on the branches, in the following order: ML/NJ/MP. Sequences are labelled by their mnemonics, see also Table S2 for details.

Mentions: Clusters of eight genes encoding the typical F1F0 ATPase have been identified in all mollicutes with the exception of plant pathogenic phytoplasmas. Extra copies of atpA (subunit α, F1-sector) and atpD (subunit β, F1-sector) genes, organized in pairs, have also been annotated in several mycoplasma genomes. Blastp queries have identified such extra copies in many species (Figure 2A). In the Hominis phylogenetic group which includes mycoplasmas pathogenic to humans and various animals, all eight of the available genomes contain one to three extra copies of the atpA-like/atpD-like gene pair. In the Pneumoniae group which also contains human and animal pathogens, two of the five species had extra copies. One extra pair of genes was found in the genome of the human urogenital pathogen Ureaplasma parvum (serovar 3 strain ATCC 700970) and in the other two complete Ureaplasma genomes available (serovar 3 strain ATCC 27815 and serovar 10 strain ATCC 33699, not shown). In the genome of the bird pathogen Mycoplasma gallisepticum, one pair of atpA-like/atpD-like genes was found. An additional gene related to atpD was also detected at another locus on the chromosome. Within the Spiroplasma phylogenetic group, an extra pair of genes was found in the genomes of the ruminant pathogens Mmm, Mycoplasma mycoides subsp. capri and Mycoplasma capricolum subsp. capricolum. By contrast, no extra copies of genes related to the F1F0 ATPase were predicted in the genomes of Mesoplasma florum (isolated from the surface of a lemon tree flower) and Spiroplasma citri (plant pathogen transmitted by insects). All the proteins encoded by the additional atpA-like and atpD-like genes were predicted to contain the corresponding Prosite motif (PS00152 ATPASE ALPHA BETA) and most were annotated accordingly.


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)

Distribution and evolution of extra copies of atpA-like and atpD-like genes in mollicutes.A. The number of typical F1F0 ATPase operons and of extra copies of atpA-like/atpD-like pairs of genes are indicated for each species. * In M. gallisepticum, one of the two extra copies only contains a truncated atpD-like gene. The 16S rDNA phylogenetic tree was generated by the ML method; bootstrap values of more than 50% are indicated. Bacillus subtilis was chosen as an outgroup species. Phylogenetic groups are indicated: S, Spiroplasma; H, Hominis; P, Pneumoniae; AP, Acholeplasma/Phytoplasma. Mnemonic codes are indicated in brackets besides species names when useful. B. The amino acid sequences of the proteins encoded by the atpA-like and atpD-like genes were concatenated and a multiple alignment was generated. Protein sequences of Type 1 atpA and atpD genes from M. pulmonis and B. subtilis (GenBank ID: atpA, NP_391564.1; atpD, NP_391562.1) were used as outgroup. The multiple sequence alignment was curated with GBLOCK to remove unreliable sites and a final round of manual editing was performed with Jalview. Phylogenetic trees were generated by ML, NJ and MP methods. The tree represented was obtained by the ML method. The aLRT/Bootstrap values corresponding to these three methods are indicated on the branches, in the following order: ML/NJ/MP. Sequences are labelled by their mnemonics, see also Table S2 for details.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3369863&req=5

pone-0038793-g002: Distribution and evolution of extra copies of atpA-like and atpD-like genes in mollicutes.A. The number of typical F1F0 ATPase operons and of extra copies of atpA-like/atpD-like pairs of genes are indicated for each species. * In M. gallisepticum, one of the two extra copies only contains a truncated atpD-like gene. The 16S rDNA phylogenetic tree was generated by the ML method; bootstrap values of more than 50% are indicated. Bacillus subtilis was chosen as an outgroup species. Phylogenetic groups are indicated: S, Spiroplasma; H, Hominis; P, Pneumoniae; AP, Acholeplasma/Phytoplasma. Mnemonic codes are indicated in brackets besides species names when useful. B. The amino acid sequences of the proteins encoded by the atpA-like and atpD-like genes were concatenated and a multiple alignment was generated. Protein sequences of Type 1 atpA and atpD genes from M. pulmonis and B. subtilis (GenBank ID: atpA, NP_391564.1; atpD, NP_391562.1) were used as outgroup. The multiple sequence alignment was curated with GBLOCK to remove unreliable sites and a final round of manual editing was performed with Jalview. Phylogenetic trees were generated by ML, NJ and MP methods. The tree represented was obtained by the ML method. The aLRT/Bootstrap values corresponding to these three methods are indicated on the branches, in the following order: ML/NJ/MP. Sequences are labelled by their mnemonics, see also Table S2 for details.
Mentions: Clusters of eight genes encoding the typical F1F0 ATPase have been identified in all mollicutes with the exception of plant pathogenic phytoplasmas. Extra copies of atpA (subunit α, F1-sector) and atpD (subunit β, F1-sector) genes, organized in pairs, have also been annotated in several mycoplasma genomes. Blastp queries have identified such extra copies in many species (Figure 2A). In the Hominis phylogenetic group which includes mycoplasmas pathogenic to humans and various animals, all eight of the available genomes contain one to three extra copies of the atpA-like/atpD-like gene pair. In the Pneumoniae group which also contains human and animal pathogens, two of the five species had extra copies. One extra pair of genes was found in the genome of the human urogenital pathogen Ureaplasma parvum (serovar 3 strain ATCC 700970) and in the other two complete Ureaplasma genomes available (serovar 3 strain ATCC 27815 and serovar 10 strain ATCC 33699, not shown). In the genome of the bird pathogen Mycoplasma gallisepticum, one pair of atpA-like/atpD-like genes was found. An additional gene related to atpD was also detected at another locus on the chromosome. Within the Spiroplasma phylogenetic group, an extra pair of genes was found in the genomes of the ruminant pathogens Mmm, Mycoplasma mycoides subsp. capri and Mycoplasma capricolum subsp. capricolum. By contrast, no extra copies of genes related to the F1F0 ATPase were predicted in the genomes of Mesoplasma florum (isolated from the surface of a lemon tree flower) and Spiroplasma citri (plant pathogen transmitted by insects). All the proteins encoded by the additional atpA-like and atpD-like genes were predicted to contain the corresponding Prosite motif (PS00152 ATPASE ALPHA BETA) and most were annotated accordingly.

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