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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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Genomic contexts of Type 2 and Type 3 clusters in mycoplasmas.Homologous genes are indicated by boxes of the same colour, connected by dashed lines. The genomic regions containing the Type 2 (A) and Type 3 (B) clusters are framed in red. The schematic diagram was generated from screenshots obtained from the MBGD database. Mnemonics and gene names are indicated; genes from the clusters are numbered arbitrarily from 1 to 7. The genome structures of M. mycoides subsp. capri and M. capricolum subsp. capricolum were identical to that of Mmm.
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pone-0038793-g005: Genomic contexts of Type 2 and Type 3 clusters in mycoplasmas.Homologous genes are indicated by boxes of the same colour, connected by dashed lines. The genomic regions containing the Type 2 (A) and Type 3 (B) clusters are framed in red. The schematic diagram was generated from screenshots obtained from the MBGD database. Mnemonics and gene names are indicated; genes from the clusters are numbered arbitrarily from 1 to 7. The genome structures of M. mycoides subsp. capri and M. capricolum subsp. capricolum were identical to that of Mmm.

Mentions: We analysed the genomic context of Type 2 and Type 3 atpA-like and atpD-like genes. A genomic region surrounding Type 2 atpA-like/atpD-like genes and including nine syntenic genes was common to M. mobile and M. pulmonis (Figure 5A). Two genes located downstream from the atpA-like/atpD-like genes encoded a phosphate acetyltransferase (eutD) and an acetate kinase (ack). These tandemly associated genes were found at various locations on the chromosomes of most mycoplasmas, whether or not atpA-like/atpD-like genes were present. By contrast, the five genes upstream from the atpA-like/atpD-like genes encoded conserved hypothetical proteins. None presented homologs that could be identified by blastp search in other mollicutes or any other organism. These genes are listed in Table S2. For convenience, the seven genes of the cluster were arbitrarily numbered 1 to 7. Gene 5 of the Type 2 cluster in strain UABCTIP of M. pulmonis was interrupted by a stop codon [42], as confirmed by PCR and sequencing. However, this mutation was not found in other three strains of M. pulmonis (not shown).


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)

Genomic contexts of Type 2 and Type 3 clusters in mycoplasmas.Homologous genes are indicated by boxes of the same colour, connected by dashed lines. The genomic regions containing the Type 2 (A) and Type 3 (B) clusters are framed in red. The schematic diagram was generated from screenshots obtained from the MBGD database. Mnemonics and gene names are indicated; genes from the clusters are numbered arbitrarily from 1 to 7. The genome structures of M. mycoides subsp. capri and M. capricolum subsp. capricolum were identical to that of Mmm.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0038793-g005: Genomic contexts of Type 2 and Type 3 clusters in mycoplasmas.Homologous genes are indicated by boxes of the same colour, connected by dashed lines. The genomic regions containing the Type 2 (A) and Type 3 (B) clusters are framed in red. The schematic diagram was generated from screenshots obtained from the MBGD database. Mnemonics and gene names are indicated; genes from the clusters are numbered arbitrarily from 1 to 7. The genome structures of M. mycoides subsp. capri and M. capricolum subsp. capricolum were identical to that of Mmm.
Mentions: We analysed the genomic context of Type 2 and Type 3 atpA-like and atpD-like genes. A genomic region surrounding Type 2 atpA-like/atpD-like genes and including nine syntenic genes was common to M. mobile and M. pulmonis (Figure 5A). Two genes located downstream from the atpA-like/atpD-like genes encoded a phosphate acetyltransferase (eutD) and an acetate kinase (ack). These tandemly associated genes were found at various locations on the chromosomes of most mycoplasmas, whether or not atpA-like/atpD-like genes were present. By contrast, the five genes upstream from the atpA-like/atpD-like genes encoded conserved hypothetical proteins. None presented homologs that could be identified by blastp search in other mollicutes or any other organism. These genes are listed in Table S2. For convenience, the seven genes of the cluster were arbitrarily numbered 1 to 7. Gene 5 of the Type 2 cluster in strain UABCTIP of M. pulmonis was interrupted by a stop codon [42], as confirmed by PCR and sequencing. However, this mutation was not found in other three strains of M. pulmonis (not shown).

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