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. 2024 Oct 14;22(10):e3002814.
doi: 10.1371/journal.pbio.3002814. eCollection 2024 Oct.

Intragenomic conflicts with plasmids and chromosomal mobile genetic elements drive the evolution of natural transformation within species

Fanny Mazzamurro  1   2 , Jason Baby Chirakadavil  3 , Isabelle Durieux  3 , Ludovic Poiré  3 , Julie Plantade  3 , Christophe Ginevra  4 , Sophie Jarraud  4 , Gottfried Wilharm  5 , Xavier Charpentier  3 , Eduardo P C Rocha  1
Affiliations

Intragenomic conflicts with plasmids and chromosomal mobile genetic elements drive the evolution of natural transformation within species

Fanny Mazzamurro et al. PLoS Biol. .

Abstract

Natural transformation is the only mechanism of genetic exchange controlled by the recipient bacteria. We quantified its rates in 786 clinical strains of the human pathogens Legionella pneumophila (Lp) and 496 clinical and environmental strains of Acinetobacter baumannii (Ab). The analysis of transformation rates in the light of phylogeny revealed they evolve by a mixture of frequent small changes and a few large quick jumps across 6 orders of magnitude. In standard conditions close to half of the strains of Lp and a more than a third in Ab are below the detection limit and thus presumably non-transformable. Ab environmental strains tend to have higher transformation rates than the clinical ones. Transitions to non-transformability were frequent and usually recent, suggesting that they are deleterious and subsequently purged by natural selection. Accordingly, we find that transformation decreases genetic linkage in both species, which might accelerate adaptation. Intragenomic conflicts with chromosomal mobile genetic elements (MGEs) and plasmids could explain these transitions and a GWAS confirmed systematic negative associations between transformation and MGEs: plasmids and other conjugative elements in Lp, prophages in Ab, and transposable elements in both. In accordance with the hypothesis of modulation of transformation rates by genetic conflicts, transformable strains have fewer MGEs in both species and some MGEs inactivate genes implicated in the transformation with heterologous DNA (in Ab). Innate defense systems against MGEs are associated with lower transformation rates, especially restriction-modification systems. In contrast, CRISPR-Cas systems are associated with higher transformation rates suggesting that adaptive defense systems may facilitate cell protection from MGEs while preserving genetic exchanges by natural transformation. Ab and Lp have different lifestyles, gene repertoires, and population structure. Nevertheless, they exhibit similar trends in terms of variation of transformation rates and its determinants, suggesting that genetic conflicts could drive the evolution of natural transformation in many bacteria.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Distribution of the transformation phenotype.
(A) Distribution of the log10-transformed average transformation rates and of the binary trait across the recombination-free rooted phylogenetic trees of A. baumannii (left) and L. pneumophila (right). sncRNA rocRp presence (dark pink) distribution is also represented across L. pneumophila phylogenetic tree. The dashed line in the log10-transformed average transformation rates distribution corresponds to the transformation rate threshold that separates transformable from non-transformable strains. Tree scale is in substitution per site. (B) Distribution of the log10-transformed average transformation rates in A. baumannii (left) and L. pneumophila (right). The red vertical line stands for the threshold between transformable and non-transformable strains. ΔcomEC Ab strain and Lp Lens strain are known non-transformable strains. AB5075 Ab strain and Lp Paris strain are among the most transformable known strains. The data underlying this figure can be found in S8 Data.
Fig 2
Fig 2. Association of the transformation phenotype on recombination.
(A) Distribution of CLRTs (Log10-transformed) in TBs. The CLRT was normalized by the length of the terminal branches in relation to the inference of changes in the phenotype for these groups to be comparable. Wilcoxon test, *: p < 0.05, **: p < 0.01, ***: p < 0.001, ****: p < 0.0001. (B) Distribution of Δr2 values in the [−0.1;0.1] interval computed in 500 nt screened windows where r2 was not null in both T and NT populations. The full span of the distributions is presented in S7 Fig. Δr2 was calculated as r2mean(NT)-r2mean(T). The data underlying Fig 2A can be found in S9 Data and Fig 2B in S10 Data. CLRT, cumulated length of recombination tract; TB, terminal branch.
Fig 3
Fig 3
Presence of genes involved in natural transformation in A. baumannii (left) and L. pneumophila (right). The genes were divided regarding their function: DNA uptake, recombination, and regulation (Rg) of transformation. The data underlying this figure can be found in S12 Data.
Fig 4
Fig 4. Volcano plots showing average effect sizes and significance of the association of the gene families with the transformation phenotype according to GWASUbin in A. baumannii and L. pneumophila.
Each circle stands for a gene family. The size of the circle depends on the number of unitigs that mapped the gene in all the samples. The value on the x-axis corresponds to the average effect size of all the unitigs mapping the gene. The y-axis indicates how significant this effect can be by representing the maximal -log10-transformed p-value adjusted for population structure (lrt-pvalue) of all the unitigs of this gene. The BH threshold (dark red line) of 0.05 is set at the lrt-pvalue that once corrected by BH is equal to 0.05. Significantly associated gene families are above the Benjamini–Hochberg (BH) threshold (red dashed line). The lower graphs (B) are similar to the ones on top (A), but gene families were colored in respect to their MGE. Only gene families whose annotation was known and that had either a strong effect size or were very significant were labeled for readability. The whole set of gene families, their p-values, effect size, and frequency is listed in S6 Data. The data underlying this figure can be found in S6 Data. GWAS, genome-wide association study; MGE, mobile genetic element.
Fig 5
Fig 5
Distribution of the number of Insertion Sequences in the bacterial chromosome per isolate in transformable and non-transformable strains in A. baumannii (left) and L. pneumophila (right). The data underlying this figure can be found in S14 Data.
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Grants and funding

This work was supported by the French Agence Nationale de la Recherche (ANR), under grant ANR-20-CE12-0004 (TransfoConflict). XC lab if funded by a grant Equipe FRM (Fondation pour la Recherche Médicale) EQU202303016268. EPCR lab is funded by a grant Equipe FRM (Fondation pour la Recherche Médicale) EQU201903007835 and by the Laboratoire d’Excellence IBEID Integrative Biology of Emerging Infectious Diseases [ANR-10-LABX-62-IBEID]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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