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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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ATPase F1F0 in mycoplasmas.A. Bacterial ATPase F1F0. B. Organization of the operon encoding the ATPase F1F0 in mycoplasmas. In E. coli and mycoplasma species, the F1F0 ATPase operon and likely the 3D structure are similar.
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pone-0038793-g001: ATPase F1F0 in mycoplasmas.A. Bacterial ATPase F1F0. B. Organization of the operon encoding the ATPase F1F0 in mycoplasmas. In E. coli and mycoplasma species, the F1F0 ATPase operon and likely the 3D structure are similar.

Mentions: All the mycoplasma genomes examined to date contain a typical complete operon encoding the eight subunits of the F1F0 ATPase (Figure 1). The F1F0 ATPase is thought to function primarily in ATP hydrolysis and maintenance of the electrochemical gradient in mycoplasmas, rather than in the generation of ATP [7]. Nevertheless, the genes encoding the subunits of this complex were considered to be essential in several species in which global transposon mutagenesis was carried out [8], [9], [10]. Surprisingly, in addition to the F1F0 ATPase operon, extra copies of atpA and atpD, organized in pairs, have been identified and annotated in many mycoplasma genomes although no specific study has ever investigated this remarkable trait. Indeed, although most bacteria have F1F0 ATPases, the presence of extra genes located outside of the traditional operon has been reported in very few cases including those encoding atypical forms of F1F0 ATPase (N-ATPases) in some marine and halotolerant bacteria, in the pathogens Burkolderia spp. and in the archaea Methanosarcina acetivorans and Methanosarcina barkeri[11]. Thus, in the general context of gene loss and redundancy elimination during the evolution of mycoplasmas, the presence of additional copies was entirely unexpected. Moreover, the prediction that these extra copies of atpA and atpD may have been exchanged during three unrelated HGT events between mycoplasmas was puzzling.


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)

ATPase F1F0 in mycoplasmas.A. Bacterial ATPase F1F0. B. Organization of the operon encoding the ATPase F1F0 in mycoplasmas. In E. coli and mycoplasma species, the F1F0 ATPase operon and likely the 3D structure are similar.
© Copyright Policy
Related In: Results  -  Collection

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

pone-0038793-g001: ATPase F1F0 in mycoplasmas.A. Bacterial ATPase F1F0. B. Organization of the operon encoding the ATPase F1F0 in mycoplasmas. In E. coli and mycoplasma species, the F1F0 ATPase operon and likely the 3D structure are similar.
Mentions: All the mycoplasma genomes examined to date contain a typical complete operon encoding the eight subunits of the F1F0 ATPase (Figure 1). The F1F0 ATPase is thought to function primarily in ATP hydrolysis and maintenance of the electrochemical gradient in mycoplasmas, rather than in the generation of ATP [7]. Nevertheless, the genes encoding the subunits of this complex were considered to be essential in several species in which global transposon mutagenesis was carried out [8], [9], [10]. Surprisingly, in addition to the F1F0 ATPase operon, extra copies of atpA and atpD, organized in pairs, have been identified and annotated in many mycoplasma genomes although no specific study has ever investigated this remarkable trait. Indeed, although most bacteria have F1F0 ATPases, the presence of extra genes located outside of the traditional operon has been reported in very few cases including those encoding atypical forms of F1F0 ATPase (N-ATPases) in some marine and halotolerant bacteria, in the pathogens Burkolderia spp. and in the archaea Methanosarcina acetivorans and Methanosarcina barkeri[11]. Thus, in the general context of gene loss and redundancy elimination during the evolution of mycoplasmas, the presence of additional copies was entirely unexpected. Moreover, the prediction that these extra copies of atpA and atpD may have been exchanged during three unrelated HGT events between mycoplasmas was puzzling.

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