Evolution of plasmid mobility: origin and fate of non-conjugative plasmids

Abstract

Conjugation drives horizontal gene transfer of many adaptive traits across prokaryotes. Yet, only a fourth of the plasmids encode the functions necessary to conjugate autonomously, others being non-mobile or mobilizable by other elements. How these different plasmids evolve is poorly understood. Here, we studied plasmid evolution in terms of their gene repertoires and relaxases. We observed that gene content in plasmid varies rapidly in relation to the rate of evolution of relaxases, such that plasmids with 95% identical relaxases have on average fewer than 50% of homologs. The identification of 249 recent transitions in terms of mobility types revealed that they are associated with even greater changes in gene repertoires, possibly mediated by transposable elements that are more abundant in such plasmids. These changes include pseudogenization of the conjugation locus, exchange of replication initiators, and extensive gene loss. In some instances, the transition between mobility types also leads to the genesis of novel plasmid taxonomic units. Most of these transitions are short-lived, suggesting a source-sink dynamic, where conjugative plasmids constantly generate mobilizable and putatively non-mobilizable plasmids by gene deletion. Yet, in few cases such transitions resulted in the emergence of large clades of relaxases present only in mobilizable plasmids, suggesting successful specialization of these families in the hijacking of diverse conjugative systems. Our results shed further light on the huge plasticity of plasmids, suggest that many non-conjugative plasmids emerged recently from conjugative elements and allowed to quantify how changes in plasmid mobility shape the variation of their gene repertoires.

Prevalence and Population Diversity of Listeria monocytogenes Isolated from Dairy Cattle Farms in the Cantabria Region of Spain

“…The conjugative transfer systems are classified in six MOB families: MOB F , MOB H , MOB Q , MOB C , MOB P and MOB V , with MOB P being the most diverse as it can be detected in plasmids from various incompatibility groups [ 86 ]. Since proteins from the MOB P conjugative transfer system is present in many conjugative and mobilizable plasmids [ 87 ] we can only hypothesize that conjugative and/or mobilizable plasmids might be present in the isolates studied, but it was not possible to detect them with the tools used.…”

Multiple relaxases contribute to the horizontal transfer of the virulence plasmids from the tumorigenic bacterium Pseudomonas syringae pv. savastanoi NCPPB 3335

“…The presence of a truncated traA gene in pB, coding for the MOB Q relaxase, indicate that this plasmid might have also originated from the fusion of two plasmids. The reason for the occurrence of multiple relaxase genes in these plasmids is intriguing, because plasmids with more than one replicon are common but only <2.6% of the 11386 plasmids analyzed in a previous work contain more than one relaxase gene (Coluzzi et al, 2022). It is possible then that the occurrence of these relaxases does not impart any selective advantage to strain NCPPB 3335 or its plasmids, but that it is only a neutral side effect of the fortuitous cointegration of plasmids to generate a surviving chimeric molecule.…”

Gene transferability and sociality do not correlate with gene connectivity

“…Around 53% of plasmids lack relaxases (i.e. non-mobilizable plasmids), thus cannot be mobilized by conjugation, but only by transformation or transduction, similar to chromosomal genes [24]. Even for mobilizable plasmids that are capable of using the genetic cassette of other conjugative plasmids, the rate of conjugation of these plasmids is still likely to be lower than that of conjugative plasmids [58][59][60].…”

“…However, not all plasmids can transfer via conjugation, and so plasmids can be divided into three broad mobility types: non-mobilizable (lowest or no mobility); mobilizable (intermediate mobility) and conjugative (highest mobility) (figure 1 a ) [22,23]. Conjugative plasmids carry all the genes necessary for their transfer [24]. Mobilizable plasmids cannot be transferred alone, but they carry enough genes to ‘hijack’ the machinery of a conjugative plasmid in the same cell [22].…”