Selfish, promiscuous and sometimes useful: how mobile genetic elements drive horizontal gene transfer in microbial populations

Abstract

Horizontal gene transfer (HGT) drives microbial adaptation but is often under the control of mobile genetic elements (MGEs) whose interests are not necessarily aligned with those of their hosts. In general, transfer is costly to the donor cell while potentially beneficial to the recipients. The diversity and plasticity of cell-MGEs interactions, and those among MGEs, result in complex evolutionary processes where the source, or even the existence of selection for maintaining a function in the genome, is often unclear. For example, MGE-driven HGT depends on cell envelope structures and defense systems, but many of these are transferred by MGEs themselves. MGEs can spur periods of intense gene transfer by increasing their own rates of horizontal transmission upon communicating, eavesdropping, or sensing the environment and the host physiology. This may result in high-frequency transfer of host genes unrelated to the MGE. Here, we review how MGEs drive HGT and how their transfer mechanisms, selective pressures and genomic traits affect gene flow, and therefore adaptation, in microbial populations. The encoding of many adaptive niche-defining microbial traits in MGEs means that intragenomic conflicts and alliances between cells and their MGEs are key to microbial functional diversification. This article is part of a discussion meeting issue 'Genomic population structures of microbial pathogens'.

Keywords: bacteriophages; defence systems; evolution; horizontal gene transfer; plasmids; satellites.

Figure 1.

Major mechanisms of HGT driven by MGEs. CONJ, conjugative element; MOB, element mobilizable by conjugation. T4SS, type IV secretion system; ICE, integrative conjugative element; IME, integrative mobilizable element.

Figure 2.

Recombination, defense and communication shape HGT. (a) Prophages protect against other phages by many mechanisms, including superinfection exclusion and repression of gene expression. (b) Plasmids can eavesdrop the quorum-sensing mechanisms of the host cell and use their own to promote their conjugation when there are many closely related hosts without plasmids in the neighbourhood of the host cell. (c) Homologous recombination requires high similarity between the exogenous DNA and the chromosome. (d) Bacteria with compatible restriction-modification (R-M) systems can exchange DNA at higher rates because the DNA is marked with the correct epigenetic markers and is not restricted by the recipient cell.

Figure 3.

(a) The capsule is a barrier to phage infection when it hides phage receptors. But some phages have evolved to degrade the capsule and can thus use it for adsorption. (b) The capsule is frequently lost and gained by HGT during K. pneumoniae evolution, resulting in frequent serotype switching. (c) Because of the capsular specificity of temperate phages in K. pneumoniae, phage-driven HGT is much more frequent within than between serotypes. By contrast, non-capsulated cells are more permissive to conjugation. Hence, gene flow depends on the presence of the capsule, its serotype and the type of MGE driving HGT.

Figure 4.

Impact of the high turn-over of MGEs on gene repertoire (left) and genome size of the host. (a) Gene repertoire relatedness decreases quickly with the patristic distance in E. coli (red spline fit line) at short evolutionary distances, i.e. between genomes of the same sequence types (ST). The subsequent changes are more moderated and approximately linear with time (black linear fit line) [103]. Of note, the variance around these average trends is very large. This figure was simplified and redrawn from the data in [103]. (b) The horizontal line is the linear regression of the fraction of accessory genes per genome as a function of the average species genome size (for the 90 most-represented species in GenBank). Figure redrawn and simplified from the results presented in [105]. B. cenocepacia, Burkholderia cenocepacia; B. longum, Bifidobacterium longum; C. trachomatis, Chlamydia trachomatis; E. coli, Escherichia coli; E. faecium, Enterococcus faecium; K. pneumoniae, Klebsiella pneumoniae; B. pertussis, Bordetella pertussis.