A widespread family of phage-inducible chromosomal islands only steals bacteriophage tails to spread in nature

Phage satellites are genetic elements that couple their life cycle to that of helper phages they parasitize, interfering with phage packaging through the production of small capsids, where only satellites are packaged. So far, in all analyzed systems, the satellite-sized capsids are composed of phage proteins. Here, we report that a family of phage-inducible chromosomal islands (PICIs), a type of satellites, encodes all the proteins required for both the production of small-sized capsids and the exclusive packaging of the PICIs into these capsids. Therefore, this new family, named capsid-forming PICIs (cf-PICIs), only requires phage tails to generate PICI particles. Remarkably, the representative cf-PICIs are produced with no cost from their helper phages, suggesting that the relationship between these elements is not parasitic. Finally, our phylogenomic studies indicate that cf-PICIs are present both in gram-positive and gram-negative bacteria and have evolved at least three times independently to spread in nature

Recruitment of a lineage-specific virulence regulatory pathway promotes intracellular infection by a plant pathogen experimentally evolved into a legume symbiont

Ajuts: We are grateful to Lidwine Trouilh for helping in NimbleGen microarray hybridizations and Loic Escoriza for mutant construction. J.P.C. and C.C. were supported by the Initiative d'Excellence IDEX UNITI Actions Thématiques Stratégiques program (RHIZOWHEAT 2014) and by the French National Research Agency (ANR-12-ADAP-0014-01). This work was supported by funds from the French National Institute for Agricultural Research (Plant Health and the Environment Division), the French National Research Agency (ANR-12-ADAP-0014-01) and the French Laboratory of Excellence project TULIP (ANR-10-LABX-41). The complete collections of events generated for all the clones from this study are available on the Microscope platform (https://www.genoscope.cns.fr/agc/microscope/expdata/NGSProjectEvo.php, SYMPA tag).Ecological transitions between different lifestyles, such as pathogenicity, mutualism and saprophytism, have been very frequent in the course of microbial evolution, and often driven by horizontal gene transfer. Yet, how genomes achieve the ecological transition initiated by the transfer of complex biological traits remains poorly known. Here we used experimental evolution, genomics, transcriptomics and high-resolution phenotyping to analyze the evolution of the plant pathogen Ralstonia solanacearum into legume symbionts, following the transfer of a natural plasmid encoding the essential mutualistic genes. We show that a regulatory pathway of the recipient R. solanacearum genome involved in extracellular infection of natural hosts was reused to improve intracellular symbiosis with the Mimosa pudica legume. Optimization of intracellular infection capacity was gained through mutations affecting two components of a new regulatory pathway, the transcriptional regulator efpR and a region upstream from the RSc0965-0967 genes of unknown functions. Adaptive mutations caused the downregulation of efpR and the over-expression of a downstream regulatory module, the three unknown genes RSc3146-3148, two of which encoding proteins likely associated to the membrane. This over-expression led to important metabolic and transcriptomic changes and a drastic qualitative and quantitative improvement of nodule intracellular infection. In addition, these adaptive mutations decreased the virulence of the original pathogen. The complete efpR/RSc3146-3148 pathway could only be identified in the genomes of the pathogenic R. solanacearum species complex. Our findings illustrate how the rewiring of a genetic network regulating virulence allows a radically different type of symbiotic interaction and contributes to ecological transitions and trade-offs

Natural Genome Diversity of AI-2 Quorum Sensing in Escherichia coli: Conserved Signal Production but Labile Signal Reception

Quorum sensing (QS) regulates the onset of bacterial social responses in function to cell density having an important impact in virulence. Autoinducer-2 (AI-2) is a signal that has the peculiarity of mediating both intra- and interspecies bacterial QS. We analyzed the diversity of all components of AI-2 QS across 44 complete genomes of Escherichia coli and Shigella strains. We used phylogenetic tools to study its evolution and determined the phenotypes of single-deletion mutants to predict phenotypes of natural strains. Our analysis revealed many likely adaptive polymorphisms both in gene content and in nucleotide sequence. We show that all natural strains possess the signal emitter (the luxS gene), but many lack a functional signal receptor (complete lsr operon) and the ability to regulate extracellular signal concentrations. This result is in striking contrast with the canonical species-specific QS systems where one often finds orphan receptors, without a cognate synthase, but not orphan emitters. Our analysis indicates that selection actively maintains a balanced polymorphism for the presence/absence of a functional lsr operon suggesting diversifying selection on the regulation of signal accumulation and recognition. These results can be explained either by niche-specific adaptation or by selection for a coercive behavior where signal-blind emitters benefit from forcing other individuals in the population to haste in cooperative behaviors.International Early Career Scientist grant from the Howard Hughes Medical Institute: (HHMI 55007436), Institut Pasteur, the CNRS, FCT award: (SFRH/BPD/26852/2006), salary support of LAO/ITQB & FCT