Conjugative plasmids: vessels of the communal gene pool

Abstract

Comparative whole-genome analyses have demonstrated that horizontal gene transfer (HGT) provides a significant contribution to prokaryotic genome innovation. The evolution of specific prokaryotes is therefore tightly linked to the environment in which they live and the communal pool of genes available within that environment. Here we use the term supergenome to describe the set of all genes that a prokaryotic 'individual' can draw on within a particular environmental setting. Conjugative plasmids can be considered particularly successful entities within the communal pool, which have enabled HGT over large taxonomic distances. These plasmids are collections of discrete regions of genes that function as 'backbone modules' to undertake different aspects of overall plasmid maintenance and propagation. Conjugative plasmids often carry suites of 'accessory elements' that contribute adaptive traits to the hosts and, potentially, other resident prokaryotes within specific environmental niches. Insight into the evolution of plasmid modules therefore contributes to our knowledge of gene dissemination and evolution within prokaryotic communities. This communal pool provides the prokaryotes with an important mechanistic framework for obtaining adaptability and functional diversity that alleviates the need for large genomes of specialized 'private genes'.

Figure 1.

Overview of the supergenome concept. The supergenome is the total pool of genes readily available to a prokaryotic organism in a particular community setting. It consists of essential genes encoded on the chromosome, termed the private pool, and genes encoded on MGEs (plasmids, transposons, viruses etc.), termed the communal pool.

Figure 2.

The modular and hierarchical composition of MGEs. Gene cassettes are inserted into integrons by integrase-mediated site-specific recombination. Integrons may be inserted into composite transposons (mobile gene islands flanked by transposase-encoding insertion sequences), which in turn may be inserted into a dispersive element like a conjugative plasmid. The plasmid thus becomes a vessel for the transportation of genetic information within the communal gene pool.

Figure 3.

Graphical representation of the mosaic structure of the ‘genetic adaptive load’ region of the IncX1 plasmid pOLA52. Two composite transposons (Tn6010 and Tn6011) have been inserted into the plasmid, which confer biofilm formation and multi-drug resistance. Both composite transposons carry foreign chromosomal regions, which can also be identified by a markedly higher average in GC composition (green curve), showing more than 99% homology to K. pneumoniae MGH 78578. The Tn6010 transposon has inserted itself within a region that has disrupted a resident Tn3 transposon without disturbing an ampicillin-resistance conferring gene (bla). Adapted from Norman et al. (2008).

Figure 4.

An overview of the organization of an archetypical conjugative plasmid comprised four gene modules: stability (blue), replication (red), propagation (green) and adaptation (orange) compared with the organization of the annotated IncX1 plasmid pOLA52 isolated from E. coli. Genes encoding unknown functions or functions not directly related to the four modules are indicated with grey.