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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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Evolutionary distance between clusters.Amino acid sequences of genes encoding α-like and β-like proteins of the Type 2 and Type 3 clusters (panels A, C and E) and α- and β-subunits of F1F0 Type 1 clusters (panels B, D and F) were concatenated and multiple alignments were generated. Multiple sequence alignments were curated with GBLOCK to remove unreliable sites and a final round of manual editing was performed with Jalview. Evolutionary distances were calculated with Type 3 pairs thought to have been exchanged through HGT as references. These distances are shown as a function of the evolutionary distance between species inferred from 16S rDNA data. The Type 3 pairs concerned were MAG2930/2940 (M. agalactiae), MHO_3130/3120 (M. hominis) and MGA_1321d (M. gallisepticum). In the last case, the analysis was based exclusively on the truncated atpD-like gene. Homologs from a phylogenetic group are circled: H, Hominis; P, Pneumoniae; S, Spiroplasma.
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pone-0038793-g004: Evolutionary distance between clusters.Amino acid sequences of genes encoding α-like and β-like proteins of the Type 2 and Type 3 clusters (panels A, C and E) and α- and β-subunits of F1F0 Type 1 clusters (panels B, D and F) were concatenated and multiple alignments were generated. Multiple sequence alignments were curated with GBLOCK to remove unreliable sites and a final round of manual editing was performed with Jalview. Evolutionary distances were calculated with Type 3 pairs thought to have been exchanged through HGT as references. These distances are shown as a function of the evolutionary distance between species inferred from 16S rDNA data. The Type 3 pairs concerned were MAG2930/2940 (M. agalactiae), MHO_3130/3120 (M. hominis) and MGA_1321d (M. gallisepticum). In the last case, the analysis was based exclusively on the truncated atpD-like gene. Homologs from a phylogenetic group are circled: H, Hominis; P, Pneumoniae; S, Spiroplasma.

Mentions: We estimated the degree of relatedness between Type 3 α-like/β-like pairs of proteins, by calculating pairwise distances between homologous pairs, using M. agalactiae, M. hominis and M. gallisepticum as references (Figure 4, panels A, C and E). For the purpose of comparison, pairwise distances were also calculated between concatenated α/β pairs from the Type 1 F1F0 ATPase (Figure 4, panels B, D and F). The F1F0 ATPase pairwise distances were roughly related to the evolutionary distance estimated on the basis of 16S rDNA pairwise distances, but no such correlation was observed for Type 3 proteins. In all cases, the minimal pairwise distances were recorded for homologs for which HGT was predicted. The most remarkable illustration of this finding concerns the isolated M. gallisepticum β-like copy (MGA_1321d), for which calculated pairwise distance from M. synoviae homolog MS53_0464 was only 0.239 whereas the other β-like copy (MGA_0491) present in M. gallisepticum was much more distant (pairwise distance: 0.613) (Figure 4E). Two additional features emerged from these graphs. First, both Type 1 and Type 2 homologs presented high pairwise distances from the Type 3 references, with the highest values obtained for Type 2 homologs. This suggests that Type 2 and Type 3 gene pairs have diverged considerably since their evolutionary separation. Second, the range of pairwise distances between homologs from the Hominis group was higher for Type 3 pairs than for F1F0 ATPase pairs. For instance, when M. agalactiae proteins were used as references, pairwise distances ranged from 0.252 to 0.625 (Δ = 0.373) for Type 3 (Figure 4A) but only from 0.234 to 0.363 (Δ = 0.129) for Type 1 (Figure 4B). Thus, even within the Hominis phylogenetic group, the level of divergence between Type 3 pairs was high, suggesting a complex evolutionary history marked by HGT and/or bursts of evolution.


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)

Evolutionary distance between clusters.Amino acid sequences of genes encoding α-like and β-like proteins of the Type 2 and Type 3 clusters (panels A, C and E) and α- and β-subunits of F1F0 Type 1 clusters (panels B, D and F) were concatenated and multiple alignments were generated. Multiple sequence alignments were curated with GBLOCK to remove unreliable sites and a final round of manual editing was performed with Jalview. Evolutionary distances were calculated with Type 3 pairs thought to have been exchanged through HGT as references. These distances are shown as a function of the evolutionary distance between species inferred from 16S rDNA data. The Type 3 pairs concerned were MAG2930/2940 (M. agalactiae), MHO_3130/3120 (M. hominis) and MGA_1321d (M. gallisepticum). In the last case, the analysis was based exclusively on the truncated atpD-like gene. Homologs from a phylogenetic group are circled: H, Hominis; P, Pneumoniae; S, Spiroplasma.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3369863&req=5

pone-0038793-g004: Evolutionary distance between clusters.Amino acid sequences of genes encoding α-like and β-like proteins of the Type 2 and Type 3 clusters (panels A, C and E) and α- and β-subunits of F1F0 Type 1 clusters (panels B, D and F) were concatenated and multiple alignments were generated. Multiple sequence alignments were curated with GBLOCK to remove unreliable sites and a final round of manual editing was performed with Jalview. Evolutionary distances were calculated with Type 3 pairs thought to have been exchanged through HGT as references. These distances are shown as a function of the evolutionary distance between species inferred from 16S rDNA data. The Type 3 pairs concerned were MAG2930/2940 (M. agalactiae), MHO_3130/3120 (M. hominis) and MGA_1321d (M. gallisepticum). In the last case, the analysis was based exclusively on the truncated atpD-like gene. Homologs from a phylogenetic group are circled: H, Hominis; P, Pneumoniae; S, Spiroplasma.
Mentions: We estimated the degree of relatedness between Type 3 α-like/β-like pairs of proteins, by calculating pairwise distances between homologous pairs, using M. agalactiae, M. hominis and M. gallisepticum as references (Figure 4, panels A, C and E). For the purpose of comparison, pairwise distances were also calculated between concatenated α/β pairs from the Type 1 F1F0 ATPase (Figure 4, panels B, D and F). The F1F0 ATPase pairwise distances were roughly related to the evolutionary distance estimated on the basis of 16S rDNA pairwise distances, but no such correlation was observed for Type 3 proteins. In all cases, the minimal pairwise distances were recorded for homologs for which HGT was predicted. The most remarkable illustration of this finding concerns the isolated M. gallisepticum β-like copy (MGA_1321d), for which calculated pairwise distance from M. synoviae homolog MS53_0464 was only 0.239 whereas the other β-like copy (MGA_0491) present in M. gallisepticum was much more distant (pairwise distance: 0.613) (Figure 4E). Two additional features emerged from these graphs. First, both Type 1 and Type 2 homologs presented high pairwise distances from the Type 3 references, with the highest values obtained for Type 2 homologs. This suggests that Type 2 and Type 3 gene pairs have diverged considerably since their evolutionary separation. Second, the range of pairwise distances between homologs from the Hominis group was higher for Type 3 pairs than for F1F0 ATPase pairs. For instance, when M. agalactiae proteins were used as references, pairwise distances ranged from 0.252 to 0.625 (Δ = 0.373) for Type 3 (Figure 4A) but only from 0.234 to 0.363 (Δ = 0.129) for Type 1 (Figure 4B). Thus, even within the Hominis phylogenetic group, the level of divergence between Type 3 pairs was high, suggesting a complex evolutionary history marked by HGT and/or bursts of evolution.

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