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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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Evolution of atpA and atpA-like genes in bacteria.The phylogenetic tree was inferred from the amino acid sequences of ATPase alpha subunits encoded by atpA and atpA-like genes. Multiple alignment was generated with MUSCLE. The phylogenetic tree was generated by the ML method. Branches corresponding to Type 1, Type 1′, Type 2 and Type 3 proteins were supported by 96–100% bootstrap values. The ML, NJ, MP and ME methods generated trees with similar topologies, except alternative branching of N-ATPases using NJ or ME (indicated by a star). Main bacterial groups are indicated. Proteins from mollicutes are named by their mnemonics, others by the species name. See Table S2 for details.
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pone-0038793-g003: Evolution of atpA and atpA-like genes in bacteria.The phylogenetic tree was inferred from the amino acid sequences of ATPase alpha subunits encoded by atpA and atpA-like genes. Multiple alignment was generated with MUSCLE. The phylogenetic tree was generated by the ML method. Branches corresponding to Type 1, Type 1′, Type 2 and Type 3 proteins were supported by 96–100% bootstrap values. The ML, NJ, MP and ME methods generated trees with similar topologies, except alternative branching of N-ATPases using NJ or ME (indicated by a star). Main bacterial groups are indicated. Proteins from mollicutes are named by their mnemonics, others by the species name. See Table S2 for details.

Mentions: We characterized the evolutionary relationship between the typical F1F0 ATPase and these extra copies of the atpA and atpD genes, by generating multiple alignments of the corresponding α-like and β-like protein sequences and inferring phylogenetic trees. A selection of F1F0 ATPase homologs from non mollicute bacteria and some related N-ATPases [11] were included in this analysis. The general shape of the tree was identical for both proteins (the tree obtained for α and α-like proteins is shown in Figure 3), indicating a clear divergence of the mycoplasma-specific extra copies from both genuine bacterial F1F0 ATPase homologs and N-ATPase homologs. Indeed, the typical F1F0 ATPase subunits from mollicutes clustered with the orthologous proteins found in most bacteria, in a sub-tree with a topology resembling that for 16S rDNA. These typical F1F0 ATPase copies and atypical N-ATPases are referred to hereafter as Type 1 and Type 1′, respectively.


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)

Evolution of atpA and atpA-like genes in bacteria.The phylogenetic tree was inferred from the amino acid sequences of ATPase alpha subunits encoded by atpA and atpA-like genes. Multiple alignment was generated with MUSCLE. The phylogenetic tree was generated by the ML method. Branches corresponding to Type 1, Type 1′, Type 2 and Type 3 proteins were supported by 96–100% bootstrap values. The ML, NJ, MP and ME methods generated trees with similar topologies, except alternative branching of N-ATPases using NJ or ME (indicated by a star). Main bacterial groups are indicated. Proteins from mollicutes are named by their mnemonics, others by the species name. See Table S2 for details.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3369863&req=5

pone-0038793-g003: Evolution of atpA and atpA-like genes in bacteria.The phylogenetic tree was inferred from the amino acid sequences of ATPase alpha subunits encoded by atpA and atpA-like genes. Multiple alignment was generated with MUSCLE. The phylogenetic tree was generated by the ML method. Branches corresponding to Type 1, Type 1′, Type 2 and Type 3 proteins were supported by 96–100% bootstrap values. The ML, NJ, MP and ME methods generated trees with similar topologies, except alternative branching of N-ATPases using NJ or ME (indicated by a star). Main bacterial groups are indicated. Proteins from mollicutes are named by their mnemonics, others by the species name. See Table S2 for details.
Mentions: We characterized the evolutionary relationship between the typical F1F0 ATPase and these extra copies of the atpA and atpD genes, by generating multiple alignments of the corresponding α-like and β-like protein sequences and inferring phylogenetic trees. A selection of F1F0 ATPase homologs from non mollicute bacteria and some related N-ATPases [11] were included in this analysis. The general shape of the tree was identical for both proteins (the tree obtained for α and α-like proteins is shown in Figure 3), indicating a clear divergence of the mycoplasma-specific extra copies from both genuine bacterial F1F0 ATPase homologs and N-ATPase homologs. Indeed, the typical F1F0 ATPase subunits from mollicutes clustered with the orthologous proteins found in most bacteria, in a sub-tree with a topology resembling that for 16S rDNA. These typical F1F0 ATPase copies and atypical N-ATPases are referred to hereafter as Type 1 and Type 1′, respectively.

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