Being Pathogenic, Plastic, and Sexual while Living with a Nearly Minimal Bacterial Genome

Pascal Sirand-Pugnet,Christine Citti,Sophie Mangenot,Chantal Schenowitz,Beatrice Segurens,Aurélien Barré,Valérie Barbe,Antoine De Daruvar,Carole Lartigue,Marc Marenda,Alain Blanchard,Daniel Jacob,Arnaud Couloux

doi:10.1371/journal.pgen.0030075

Abstract

Mycoplasmas are commonly described as the simplest self-replicating organisms, whose evolution was mainly characterized by genome downsizing with a proposed evolutionary scenario similar to that of obligate intracellular bacteria such as insect endosymbionts. Thus far, analysis of mycoplasma genomes indicates a low level of horizontal gene transfer (HGT) implying that DNA acquisition is strongly limited in these minimal bacteria. In this study, the genome of the ruminant pathogen Mycoplasma agalactiae was sequenced. Comparative genomic data and phylogenetic tree reconstruction revealed that ∼18% of its small genome (877,438 bp) has undergone HGT with the phylogenetically distinct mycoides cluster, which is composed of significant ruminant pathogens. HGT involves genes often found as clusters, several of which encode lipoproteins that usually play an important role in mycoplasma–host interaction. A decayed form of a conjugative element also described in a member of the mycoides cluster was found in the M. agalactiae genome, suggesting that HGT may have occurred by mobilizing a related genetic element. The possibility of HGT events among other mycoplasmas was evaluated with the available sequenced genomes. Our data indicate marginal levels of HGT among Mycoplasma species except for those described above and, to a lesser extent, for those observed in between the two bird pathogens, M. gallisepticum and M. synoviae. This first description of large-scale HGT among mycoplasmas sharing the same ecological niche challenges the generally accepted evolutionary scenario in which gene loss is the main driving force of mycoplasma evolution. The latter clearly differs from that of other bacteria with small genomes, particularly obligate intracellular bacteria that are isolated within host cells. Consequently, mycoplasmas are not only able to subvert complex hosts but presumably have retained sexual competence, a trait that may prevent them from genome stasis and contribute to adaptation to new hosts.

Highlights

Organisms belonging to the Mycoplasma genus are commonly described as the simplest and smallest self-replicating bacteria because of their total lack of cell wall, the paucity of their metabolic pathways, and the small size of their genome [1,2]
The recent findings of a putative conjugative plasmid in Rickettsia felis [8] and of a substantial number of prophage, transposase and mobile-DNA genes in the insect endosymbiont Wolbachia pipientis challenged this model and it was proposed that gene inflow by horizontal gene transfer (HGT) may occur in some obligate intracellular species depending on their lifestyles [9]
We showed that a significant amount of genes underwent horizontal transfer among different mycoplasma species that share the same ruminant hosts

Summary

Introduction

Organisms belonging to the Mycoplasma genus (class Mollicutes) are commonly described as the simplest and smallest self-replicating bacteria because of their total lack of cell wall, the paucity of their metabolic pathways, and the small size of their genome [1,2]. The environment is rather steady and natural selection tends to be reduced, resulting in the inactivation of many genes by genetic drift [5,6]. In this scenario, DNA acquisition would be strongly limited, resulting, after losses of large genomic regions and accumulation of mutations, in genome stasis [7]. DNA acquisition would be strongly limited, resulting, after losses of large genomic regions and accumulation of mutations, in genome stasis [7] This evolution scheme is relevant for a number of obligate intracellular bacteria, including insect endosymbionts (e.g., Buchnera and Wigglesworthia spp.), and arguably for Chlamydia, and Rickettsia spp. The recent findings of a putative conjugative plasmid in Rickettsia felis [8] and of a substantial number of prophage, transposase and mobile-DNA genes in the insect endosymbiont Wolbachia pipientis challenged this model and it was proposed that gene inflow by horizontal gene transfer (HGT) may occur in some obligate intracellular species depending on their lifestyles [9]

Methods

Results

Discussion

Conclusion