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

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.

Does Gene Translocation Accelerate the Evolution of Laterally Transferred Genes?

“…However, the possibility that IS elements are involved in gene translocation cannot be ruled out since most of the IS elements in genomes are evolutionarily young and under fast rates of turnover (Siguier et al 2006a;Wagner 2006a,b;Touchon and Rocha 2007). It has been shown that elements involved in gene transfer have undergone a decay process (Sirand-Pugnet et al 2007). Similarly, it might be possible that IS elements involved in gene translocation in this study have been deleted during evolution.…”

MIB–MIP is a mycoplasma system that captures and cleaves immunoglobulin G

“…putrefaciens group. Other HGTs of potential virulence factors have already been described among these groups (39). In urogenital human mycoplasmas, HGTs were predicted between M. hominis and the ancestor of the U. parvum/U.…”

Mobility of Plasmids

“…However, most mollicutes are not undergoing rapid genome degradation, have few pseudogenes, and have highly codingdense genomes (125). Since there is evidence that horizontal gene transfer is frequent in the clade (126), it is more parsimonious to think that they code for a simpler conjugative machinery. The largest plasmid encoding a T4SS is pSymA from Sinorhizobium meliloti 1021, which has 1.35 Mb.…”