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Horizontal distributive transfers and the extraordinary plasticity of the mycoplasma genome

Abstract : Background: Horizontal gene transfer (HGT) is one main driver of bacterial evolution. Long thought to be marginal in Mycoplasma, we recently challenged this dogma by showing the occurrence of significant HGT between ruminant mycoplasmas, and discovered an unconventional mechanism involving conjugative chromosomal transfers, not associated to mobile genetic elements. Whole sequencing of mating-progeny populations revealed the exchange of large chromosomal fragments that could affect any part of the chromosome. This finding did not conform to classical oriT-based conjugative mechanisms but resembled that found in mycobacteria, where the distributive transfer of multiple, non-contiguous genome segments from a donor to a recipient has been described. Such mechanism, if also occurring in mycoplasmas, will tremendously increase the evolutionary plasticity of their minimal genome. To address this issue, several individual mating-progeny derived from different mating-pairs or conditions were generated, sequenced and analyzed. Methods: Matings were conducted in different conditions (conjugation vs Polyethylene glycol (PEG)-cell fusion) using parents that differ in the position of the selective marker and the type of selection pressure. From these, 24 transconjugant genomes were fully sequenced by NGS and their parental inheritance was analyzed by comparative genomic. Results: Data showed that mycoplasma chromosomal transfers (MCT) were much more complex than expected and generated mosaic genomes, with an average of 15 distinct fragments of co-transferred donor DNA, reaching 30 in some cases. In a single mating, progenies could inherit up to 17% of the total size of the donor genome (29.4 to 147.9 kb), distributed in small (~ 0.05 kb) or large (64.7 kb) segments all around the recipient chromosome. Some regions displayed a micro-complexity, with multiple inherited-fragments separated by short intervals of recipient DNA. These most likely resulted from a combination of repair and recombination events, occurring between the recipient chromosome and a single molecule of introduced donor-DNA. Since more than 30 % regions flanking the transferred segments are micro-homologous regions (<30 nt), illegitimate recombination events might be involved in MCT. Genome mosaicism was independent of the parent pairs and was also observed following PEG-induced cell fusion. The level of identity of parental genomes and the selection pressure were found to have a significant impact on the complexity of the resulting hybrid genomes. Conclusion: Analyses of single progeny genomes provides new insights on the MCT mechanism and suggests that it can create high genome diversity, almost instantly: in one single event, MCT generates transconjugants that are a mosaic blend of the parental genomes reminiscent of that seen in the meiotic product of sexual reproduction. This distributive conjugative mechanism allows integration/deletion of genetic materials, but also micro-heterogeneity possibly implicated in refining/regulating functional elements. Our finding challenges the common idea that during bacterial conjugation, DNA flow is only driven by conjugative elements and brings into the spotlight a new mean for rapid bacterial innovation that is likely shared by other genus. Moreover, it emphasizes the extraordinary plasticity of the minute-size genomes of mycoplasma.
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https://hal.inrae.fr/hal-02933415
Contributor : Emilie Dordet-Frisoni Connect in order to contact the contributor
Submitted on : Tuesday, September 8, 2020 - 2:01:43 PM
Last modification on : Wednesday, November 3, 2021 - 7:24:46 AM

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  • HAL Id : hal-02933415, version 1

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Emilie Dordet-Frisoni, Christine Citti, Eveline Sagné, Laurent Xavier Nouvel, Marion Faucher. Horizontal distributive transfers and the extraordinary plasticity of the mycoplasma genome. 22th Congress of the International Organization for Mycoplasmology (IOM), IOM, Jul 2018, Portsmouth, New Hampshire, United States. ⟨hal-02933415⟩

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