The magnitude of DNA transfer between plasmids and chromosomes in Prokaryotes

Plasmids are extrachromosomal genetic elements that are abundantly found in prokaryotic organisms. Plasmids are considered a major contributor to prokaryotic genome evolution due to their ability to transfer DNA between cells and across taxonomic boundaries. Anecdotal evidence shows that genetic material can transfer between co-resident plasmids and chromosomes, either by mobile genetic elements (transposons, integrons, prophages and IS elements) or by homologous recombination. Nonetheless, a comprehensive view on the magnitude and characteristics of the transferred DNA between plasmids and chromosomes is still lacking. Here I developed a novel comparative genomics approach based on clustering of adjacent local similarity regions (BLAST and MUMmer) by segmentation into parsimonious regions of transfer events. Applying our approach to 3,264 chromosome-plasmid pairs that co-inhabit the same prokaryotic host uncovered 332,944 shared regions in 2,272 (69,6%) pairs comprising 2,272 (69,6%) plasmids and 1,157 (82,6%) chromosomes belonging to 1,157 (82,6%) isolates. The shared regions correspond to DNA transfer events that constitute 51,866 plasmid loci and 111,124 chromosomal loci. The homologous loci on each replicon had varying sequence copy number on the other replicon ranging between 1 and 457 chromosomal copies for plasmid loci and between 1 and 109 plasmid copies for chromosomal loci. The high copy number homologous loci usually correspond to transposable elements. Many plasmid loci with chromosomal homology carry complete genes (10,660 loci). Among those loci, 4,303 loci include more than one complete gene with an overall of 15,782 genes that were putatively co-transferred as pairs or longer gene clusters. Characterizing those genes, I found that the majority belong to classes of mobile genetic elements or to hypothetical proteins with unknown functions. Among genes that were laterally transferred between the plasmid and chromosome of the same cell, I also found essential genes such as RNA genes as well as beneficial genes, like antimicrobial resistance genes (AMR) with incidents of multidrug resistance introduced to the genome by plasmids. Chromosome-plasmid pairs with no sequence homology between the plasmid and chromosome, can be characterized by a lower content of coding sequence and a higher genomic complexity. Finally, I observed and characterized several events of plasmid integration into the chromosomal genome. Our results suggest a common but not very frequent DNA transfer between plasmids and chromosomes, with some exceptions. The majority of gene transfer is facilitated by mobile elements, indicating that plasmids play a role in the dissemination of transposons much more than they do antibiotic resistance. My results implicate plasmids as mediators of transposon invasion of prokaryotic genomes.


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