High diversity and variability of pipolins among a wide range of pathogenic Escherichia coli strains
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Published on: December 23, 2022
Saskia-Camille Flament-Simon1, María de Toro2, Liubov Chuprikova3
1Laboratorio de Referencia de E. Coli (LREC), Departamento de Microbiología y Parasitología, Facultad de Veterinaria, Universidad de Santiago de Compostela (USC), 27002, Lugo, Spain.
Abstract:
Self-synthesizing transposons are integrative mobile genetic elements (MGEs) that encode their own B-family DNA polymerase (PolB). Discovered a few years ago, they are proposed as key players in the evolution of several groups of DNA viruses and virus-host interaction machinery. Pipolins are the most recent addition to the group, are integrated in the genomes of bacteria from diverse phyla and also present as circular plasmids in mitochondria. Remarkably, pipolins-encoded PolBs are proficient DNA polymerases endowed with DNA priming capacity, hence the name, primer-independent PolB (piPolB). We have now surveyed the presence of pipolins in a collection of 2,238 human and animal pathogenic Escherichia coli strains and found that, although detected in only 25 positive isolates (1.1%), they are present in E. coli strains from a wide variety of pathotypes, serotypes, phylogenetic groups and sequence types. Overall, the pangenome of strains carrying pipolins is highly diverse, despite the fact that a considerable number of strains belong to only three clonal complexes (CC10, CC23 and CC32). Comparative analysis with a set of 67 additional pipolin-harboring genomes from GenBank database spanning strains from diverse origin, further confirmed these results. The genetic structure of pipolins shows great flexibility and variability, with the piPolB gene and the attachment sites being the only common features. Most pipolins contain one or more recombinases that would be involved in excision/integration of the element in the same conserved tRNA gene. This mobilization mechanism might explain the apparent incompatibility of pipolins with other integrative MGEs such as integrons. In addition, analysis of cophylogeny between pipolins and pipolin-harboring strains showed a lack of congruence between several pipolins and their host strains, in agreement with horizontal transfer between hosts. Overall, these results indicate that pipolins can serve as a vehicle for genetic transfer among circulating E. coli and possibly also among other pathogenic bacteria.
Insights
Pipolins, mobile genetic elements encoding primer-independent DNA polymerases (piPolB), were found in 1.1% of pathogenic Escherichia coli strains. These elements exhibit genetic flexibility and horizontal transfer, suggesting a role in bacterial genetic exchange.
Area of Science:
- Microbiology
- Genetics
- Molecular Biology
Background:
- Self-synthesizing transposons are mobile genetic elements encoding DNA polymerase B (PolB).
- Pipolins are a recently identified group of these elements, found in diverse bacterial genomes and mitochondrial plasmids.
- Pipolin-encoded PolBs (piPolBs) possess unique primer-independent DNA synthesis capabilities.
Purpose of the Study:
- To investigate the prevalence and characteristics of pipolins in pathogenic Escherichia coli.
- To understand the genetic structure and mobility of pipolins within E. coli.
- To assess the potential role of pipolins in horizontal gene transfer among bacteria.
Main Methods:
- Surveyed 2,238 pathogenic E. coli strains for pipolin presence.
- Conducted comparative genomic analysis of pipolin-harboring strains from the study and GenBank.
- Analyzed pipolin genetic structure, including genes, attachment sites, and recombinases.
- Performed cophylogenetic analysis to infer horizontal transfer events.
Main Results:
- Pipolins were detected in 25 (1.1%) E. coli isolates across various pathotypes and phylogenetic groups.
- Pipolin-harboring E. coli strains displayed diverse pangenomes, with some clustering in specific clonal complexes.
- Pipolins showed genetic flexibility, with piPolB and attachment sites as conserved features; recombinases were frequently present.
- Cophylogenetic analysis indicated frequent horizontal transfer of pipolins between E. coli strains.
Conclusions:
- Pipolins are present in pathogenic E. coli, albeit at a low frequency.
- Pipolins possess a flexible genetic structure and utilize recombinases for integration, potentially explaining their incompatibility with other mobile genetic elements.
- Evidence suggests pipolins facilitate genetic transfer within E. coli populations and possibly other pathogenic bacteria.
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