Pseudogenes in plasmid genomes reveal past transitions in plasmid mobility

Abstract

Evidence for gene non-functionalization due to mutational processes is found in genomes in the form of pseudogenes. Pseudogenes are known to be rare in prokaryote chromosomes, with the exception of lineages that underwent an extreme genome reduction (e.g., obligatory pathogens). Much less is known about the frequency of pseudogenes in prokaryotic plasmids; those are genetic elements that can transfer between cells and may encode beneficial traits for their host. Non-functionalization of plasmid-encoded genes may alter the plasmid characteristics, e.g., mobility, or their effect on the host. Analyzing 10,832 prokaryotic genomes, we find that plasmid genomes are characterized by threefold-higher pseudogene density compared to chromosomes. The majority of plasmid pseudogenes correspond to deteriorated transposable elements. A detailed analysis of enterobacterial plasmids furthermore reveals frequent gene non-functionalization events associated with the loss of plasmid self-transmissibility. Reconstructing the evolution of closely related plasmids revealed that non-functionalization of the conjugation machinery led to the emergence of non-mobilizable plasmid types. Examples are virulence plasmids inEscherichiaandSalmonella. Our study highlights non-functionalization of core plasmid mobility functions as one route for the evolution of domesticated plasmids. Pseudogenes in plasmids supply insights into past transitions in plasmid mobility that are akin to transitions in bacterial lifestyle.

Identification of novel origins of transfer across bacterial plasmids

“…Interestingly, 20% of pNTs belong to PTUs where most of the plasmids are either pCONJ or pMOB (Figure S12). They could result from the latter by gene loss 25,32 . In E. coli the few remaining pNTs cover a narrow size distribution (~2 Kb and ~90Kb), which suggests the presence of a few families of abundant non-transmissible plasmids.…”

Hijackers, hitchhikers, or co-drivers? The mysteries of microbial mobilizable genetic elements

“…This has been most extensively described in mobilizable plasmids which can emerge by the loss of conjugaeon-related genes. The phylogeny of the most frequent relaxases shows that conjugaeve elements are ancestral, but very open, by gene loss, give rise to plasmids with defeceve conjugaeon systems that can only be mobilized in trans (44,112). As for MITES and CALIN, the current paradigm is that they emerge by gene deleeon: loss of the transposase for the former (113) and IS-mediated translocaeon of the integrase for the lager (35).…”