Abstract

F1F0 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 F1F0 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 F1 ATPases and could form an F1-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 F1-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 F1-like ATPases with no known equivalent in other bacteria. We propose a model, in which the F1-like structure is associated with a hypothetical X0 sector located in the membrane of mycoplasma cells.

Highlights

  • Mycoplasmas are small bacteria that infect humans and animals and evolved from low-GC content firmicutes in a process involving a drastic reduction of genome size, resulting in present-day species with typical 1 Mb-genomes [1]

  • In the species infecting birds and ruminants, several genes thought to have been subject to horizontal gene transfers (HGT) were parts of typical mobile elements including integrative conjugative elements (ICEs), insertion sequences (ISs) and restriction-modification systems (RMSs) but many others encoded transporters, lipoproteins and hypothetical proteins potentially involved in host-specificity and pathogenicity

  • Extra copies of genes related to F1F0 ATPase subunits alpha and beta are found in mycoplasma genomes

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Summary

Introduction

Mycoplasmas are small bacteria that infect humans and animals and evolved from low-GC content firmicutes in a process involving a drastic reduction of genome size, resulting in present-day species with typical 1 Mb-genomes [1]. The repertoires of genes encoding membrane proteins such as lipoproteins and transporters are highly diverse in mycoplasmas, probably reflecting the ability of the different species to infect animal species as diverse as mammals, birds, fishes and arthropods. In the species infecting birds and ruminants, several genes thought to have been subject to HGT were parts of typical mobile elements including integrative conjugative elements (ICEs), insertion sequences (ISs) and restriction-modification systems (RMSs) but many others encoded transporters, lipoproteins and hypothetical proteins potentially involved in host-specificity and pathogenicity. The genes thought to have been subject to HGT in human urogenital species encoded ISs, RMSs, hypothetical proteins and two proteins related to F1F0 ATPase subunits a (atpA)

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