Evolution of temperate phages of enterobacteria

L'intégration et la dégradation des virus (ou phages) au sein des génomes bactériens (alors nommés prophages) constituent un flux de gènes promouvant la diversification génétique de leurs hôtes. Les mécanismes à l'origine de l'impact évolutif des prophages sur leurs hôtes restent cependant mal compris. La première partie de la thèse s'est attachée à comprendre comment les prophages sont adaptés aux contraintes liées à l'organisation génétique et structurelle des chromosomes d'Escherichia et de Salmonella. Ces résultats ont mis en évidence une forte conservation des positions d'intégration des prophages, ainsi que différentes adaptations des phages à l'organisation chromosomique hôte. L'origine de la diversité génétique des phages tempérés a été au centre de la deuxième partie de la thèse. L'étude des phages lambdoïdes a révélé l'existence de deux stratégies de recombinaison chez ces phages: utilisation du système de recombinaison RecBCD de l'hôte via la présence de sites Chi ou utilisation de leur propre système de recombinaison. Ceci suggère que l'utilisation de l'une ou l'autre des stratégies a un impact important sur la diversification et le mosaïcisme génomique phagique. Enfin, la détection et l'analyse de prophages hérités verticalement au sein des génomes hôtes ont montré que de nombreux prophages partiellement dégradés sont conservés et évoluent sous sélection purificatrice. Ces résultats suggèrent que de nombreux prophages sont potentiellement des éléments fonctionnels domestiqués par la bactérie. L'ensemble de ces analyses permet de préciser les mécanismes permettant aux prophages de contribuer à la diversification des répertoires de gènes de leurs hôtes.The integration and degradation of viruses (or phages) constitute a genetic influx of genes within bacterial genomes (then named prophages). This process is thought to promote bacterial diversification. The mechanisms promoting the evolutionary impact of prophages on their hosts remain poorly understood. The first part of my thesis focused on the adaptation of prophages to the genetic and structural organization of the chromosome of Escherichia and Salmonella. These results showed a strong conservation of prophage integration positions and different adaptations of prophages to the chromosome organization of their hosts. In a second study, I focused on the mechanisms of genetic diversification of phages. The study of lambdoid phages revealed the existence of two recombination strategies among these phages: using the host recombination system RecBCD through the presence of Chi sites or using their own recombination system. This work suggests that using one or the other recombination strategy has an important impact on the genomic diversification and mosaicism of these phages. Finally, by detecting and analyzing vertically inherited prophages within their host genomes, I showed that many degraded prophages are conserved and evolve under purifying selection. This suggests that many prophages are potentially domesticated by bacteria. Altogether, these analyses are improving our understanding of the contribution of prophages to the genetic diversification of their hosts

L'évolution des phages tempérés d'entérobactéries

The integration and degradation of viruses (or phages) constitute a genetic influx of genes within bacterial genomes (then named prophages). This process is thought to promote bacterial diversification. The mechanisms promoting the evolutionary impact of prophages on their hosts remain poorly understood. The first part of my thesis focused on the adaptation of prophages to the genetic and structural organization of the chromosome of Escherichia and Salmonella. These results showed a strong conservation of prophage integration positions and different adaptations of prophages to the chromosome organization of their hosts. In a second study, I focused on the mechanisms of genetic diversification of phages. The study of lambdoid phages revealed the existence of two recombination strategies among these phages: using the host recombination system RecBCD through the presence of Chi sites or using their own recombination system. This work suggests that using one or the other recombination strategy has an important impact on the genomic diversification and mosaicism of these phages. Finally, by detecting and analyzing vertically inherited prophages within their host genomes, I showed that many degraded prophages are conserved and evolve under purifying selection. This suggests that many prophages are potentially domesticated by bacteria. Altogether, these analyses are improving our understanding of the contribution of prophages to the genetic diversification of their hosts.L'intégration et la dégradation des virus (ou phages) au sein des génomes bactériens (alors nommés prophages) constituent un flux de gènes promouvant la diversification génétique de leurs hôtes. Les mécanismes à l'origine de l'impact évolutif des prophages sur leurs hôtes restent cependant mal compris. La première partie de la thèse s'est attachée à comprendre comment les prophages sont adaptés aux contraintes liées à l'organisation génétique et structurelle des chromosomes d'Escherichia et de Salmonella. Ces résultats ont mis en évidence une forte conservation des positions d'intégration des prophages, ainsi que différentes adaptations des phages à l'organisation chromosomique hôte. L'origine de la diversité génétique des phages tempérés a été au centre de la deuxième partie de la thèse. L'étude des phages lambdoïdes a révélé l'existence de deux stratégies de recombinaison chez ces phages: utilisation du système de recombinaison RecBCD de l'hôte via la présence de sites Chi ou utilisation de leur propre système de recombinaison. Ceci suggère que l'utilisation de l'une ou l'autre des stratégies a un impact important sur la diversification et le mosaïcisme génomique phagique. Enfin, la détection et l'analyse de prophages hérités verticalement au sein des génomes hôtes ont montré que de nombreux prophages partiellement dégradés sont conservés et évoluent sous sélection purificatrice. Ces résultats suggèrent que de nombreux prophages sont potentiellement des éléments fonctionnels domestiqués par la bactérie. L'ensemble de ces analyses permet de préciser les mécanismes permettant aux prophages de contribuer à la diversification des répertoires de gènes de leurs hôtes

Evolution of Chi motifs in Proteobacteria

AbstractHomologous recombination is a key pathway found in nearly all bacterial taxa. The recombination complex not only allows bacteria to repair DNA double-strand breaks but also promotes adaption through the exchange of DNA between cells. In Proteobacteria, this process is mediated by the RecBCD complex, which relies on the recognition of a DNA motif named Chi to initiate recombination. The Chi motif has been characterized in Escherichia coliE. coliHaemophilus influenzaeBacillus subtilisLactococcus lactisStaphylococcus aureusE. coliEnterobacteriacea

Factors driving effective population size and pan-genome evolution in bacteria

Abstract Background Knowledge of population-level processes is essential to understanding the efficacy of selection operating within a species. However, attempts at estimating effective population sizes (Ne) are particularly challenging in bacteria due to their extremely large census populations sizes, varying rates of recombination and arbitrary species boundaries. Results In this study, we estimated Ne for 153 species (152 bacteria and one archaeon) defined under a common framework and found that ecological lifestyle and growth rate were major predictors of Ne; and that contrary to theoretical expectations, Ne was unaffected by recombination rate. Additionally, we found that Ne shapes the evolution and diversity of total gene repertoires of prokaryotic species. Conclusion Together, these results point to a new model of genome architecture evolution in prokaryotes, in which pan-genome sizes, not individual genome sizes, are governed by drift-barrier evolution

The Evolution of Bacterial Genome Architecture

The genome architecture of bacteria and eukaryotes evolves in opposite directions when subject to genetic drift, a difference that can be ascribed to the fact that bacteria exhibit a mutational bias that deletes superfluous sequences, whereas eukaryotes are biased toward large insertions. Expansion of eukaryotic genomes occurs through the addition of non-functional sequences, such as repetitive sequences and transposable elements, whereas variation in bacterial genome size is largely due to the acquisition and loss of functional accessory genes. These properties create the situation in which eukaryotes with very similar numbers of genes can have vastly different genome sizes, while in bacteria, gene number scales linearly with genome size. Some bacterial genomes, however, particularly those of species that undergo bottlenecks due to recent association with hosts, accumulate pseudogenes and mobile elements, conferring them a low gene content relative to their genome size. These non-functional sequences are gradually eroded and eliminated after long-term association with hosts, with the result that obligate symbionts have the smallest genomes of any cellular organism. The architecture of bacterial genomes is shaped by complex and diverse processes, but for most bacterial species, genome size is governed by a non-adaptive process, i.e., genetic drift coupled with a mutational bias toward deletions. Thus, bacteria with small effective population sizes typically have the smallest genomes. Some marine bacteria counter this near-universal trend: despite having immense population sizes, selection, not drift, acts to reduce genome size in response to metabolic constraints in their nutrient-limited environment

The chromosomal accommodation and domestication of mobile genetic elements

International audienceProkaryotes are constantly being infected by large mobile genetic elements such as conjugative elements and temperate phages. The fitness of these elements is tightly linked with the evolutionary success of the host. This leads to selection against disruptive effects their integration might have on the organization and structure of the chromosome. Seamless genetic accommodation of the mobile elements also involves silencing infectious mechanisms and expressing functions adaptive to the host

Recombination events are concentrated in the spike protein region of Betacoronaviruses.

The Betacoronaviruses comprise multiple subgenera whose members have been implicated in human disease. As with SARS, MERS and now SARS-CoV-2, the origin and emergence of new variants are often attributed to events of recombination that alter host tropism or disease severity. In most cases, recombination has been detected by searches for excessively similar genomic regions in divergent strains; however, such analyses are complicated by the high mutation rates of RNA viruses, which can produce sequence similarities in distant strains by convergent mutations. By applying a genome-wide approach that examines the source of individual polymorphisms and that can be tested against null models in which recombination is absent and homoplasies can arise only by convergent mutations, we examine the extent and limits of recombination in Betacoronaviruses. We find that recombination accounts for nearly 40% of the polymorphisms circulating in populations and that gene exchange occurs almost exclusively among strains belonging to the same subgenus. Although experimental studies have shown that recombinational exchanges occur at random along the coronaviral genome, in nature, they are vastly overrepresented in regions controlling viral interaction with host cells

Pan genomes of the lambdoid phages encoding recombination functions (Rec⁺) are larger than those lacking them (Rec⁻).

<p>The pan genome size (y-axis) of each type of phage genome was computed for increasing numbers of genomes (x-axis). For each value of x we draw x genomes randomly and compute the pan genome. This is repeated 1000 times for each value of x to draw the 95% interval of confidence of the pan genome size (grey zone).</p