The<i>Pseudomonas aeruginosa</i>Pan-Genome Provides New Insights on Its Population Structure, Horizontal Gene Transfer, and Pathogenicity

Freschi, Luca; Vincent, Antony T.; Jeukens, Julie; Emond-Rhéault, Jean-Guillaume; Kukavica-Ibrulj, Iréna; Dupont, Marie-Josée; Charette, Steve J.; Boyle, Brian; Levesque, Roger C.

doi:10.1093/gbe/evy259

Cited by 246 publications

(290 citation statements)

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“…We analyzed public available genome sequencing data on a collection of 1,139 isolates that have previously been included in a pan-and core genome analysis by Freschi et al (2019) [19], to compare the pan-and core genome sizes between different collections of isolates. When we used the same method as for our own isolate collection (GenAPI), we found that the 1,139 isolates from Pan-and core genomes…”

Section: Core Genome Snp Distances To Define Clone Typesmentioning

confidence: 99%

Gene loss and acquisition in lineages of bacteria evolving in a human host environment

Gabrielaitė

Molin

et al. 2020

Preprint

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While genome analyses have documented that there are differences in the gene repertoire between evolutionary distant lineages of the same bacterial species, less is known about micro-evolutionary dynamics of gene loss and acquisition within lineages of bacteria as they evolve over the timescale of years. This knowledge is valuable to understand both the basic mutational steps that on long timescales lead to evolutionary distant bacterial lineages, and the evolution of the individual lineages themselves.In the case that lineages evolve in a human host environment, gene loss and acquisition may furthermore have implication for disease.We analyzed the genomes of 45 Pseudomonas aeruginosa lineages evolving in the lungs of cystic fibrosis patients to identify genes that are lost or acquired during the first years of infection in each of the different lineages. On average, the lineage genome content changed with 88 genes (range 0-473). Genes were more often lost than acquired, and prophage genes were more variable than bacterial genes. We identified genes that were lost or acquired independently across different clonal lineages, i.e. convergent molecular evolution. Convergent evolution suggests that there is a selection for loss and acquisition of certain genes in the host environment. We find that a significant proportion of such genes are associated with virulence; a trait previously shown to be important for adaptation. Furthermore, we also compared the genomes across lineages to show that within-lineage variable genes more often belonged to genomic content not shared across all lineages. Finally, we used 4,760 genes shared by 446 P. aeruginosa genomes to develop a stable and discriminatory typing scheme for P. aeruginosa clone types (Pactyper, https://github.com/MigleSur/Pactyper). In sum, our analysis adds to the knowledge on the pace and drivers of gene loss and acquisition in bacteria evolving over multiple years in a human host environment 3 and provides a basis to further understand how gene loss and acquisition plays a role in lineage differentiation and host adaptation.

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Section: Core Genome Snp Distances To Define Clone Typesmentioning

confidence: 99%

Gene loss and acquisition in lineages of bacteria evolving in a human host environment

Gabrielaitė

Molin

et al. 2020

Preprint

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“…A cohort of 558 clinical and 172 environmental genome assemblies of P. aeruginosa isolates from multiple countries were used in this study (Table S2) (78,79). Clinical isolates were from patients with cystic fibrosis, bronchiectasis or chronic obstructive pulmonary disease.…”

Section: Clinical and Environmental Isolates Of P Aeruginosamentioning

confidence: 99%

“…Genome assemblies of clinical and environmental isolates have been described previously (78,79) (Table S2). For experimentally evolved mutants and clinical isolates sequenced in this study, genomic DNA was extracted from overnight cultures of endpoint resistant mutants using the MoBio UltraClean® Microbial DNA isolation kit.…”

Section: Whole Genome Sequencingmentioning

confidence: 99%

A large-scale comparison shows that genetic changes causing antibiotic resistance in experimentally evolvedPseudomonas aeruginosapredict those in naturally evolved bacteria

Wardell¹,

Rehman²,

Martin³

et al. 2019

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Pseudomonas aeruginosa is an opportunistic pathogen that causes a wide range of acute and chronic infections. An increasing number of isolates have acquired mutations that make them antibiotic resistant, making treatment more difficult. To identify resistance-associated mutations we experimentally evolved the antibiotic sensitive strain P. aeruginosa PAO1 to become resistant to three widely used anti-pseudomonal antibiotics, ciprofloxacin, meropenem and tobramycin. Mutants were able to tolerate up to 2048-fold higher concentrations of antibiotic than strain PAO1. Genome sequences were determined for thirteen mutants for each antibiotic. Each mutant had between 2 and 8 mutations. There were at least 8 genes mutated in more than one mutant per antibiotic, demonstrating the complexity of the genetic basis of resistance. Additionally, large deletions of up to 479kb arose in multiple meropenem resistant mutants. For all three antibiotics mutations arose in genes known to be associated with resistance, but also in genes not previously associated with resistance. To determine the clinical relevance of mutations uncovered in experimentallyevolved mutants we analysed the corresponding genes in 457 isolates of P. aeruginosa from patients with cystic fibrosis or bronchiectasis as well as 172 isolates from the general environment. Many of the genes identified through experimental evolution had changes predicted to be function-altering in clinical isolates but not in isolates from the general environment, showing that mutated genes in experimentally evolved bacteria can predict those that undergo mutation during infection. These findings expand understanding of the genetic basis of antibiotic resistance in P. aeruginosa as well as demonstrating the validity of experimental evolution in identifying clinically-relevant resistance-associated mutations.' ImportanceThe rise in antibiotic resistant bacteria represents an impending global health crisis. As such, understanding the genetic mechanisms underpinning this resistance can be a crucial piece of the puzzle to combatting it. The importance of this research is that by experimentally evolving P. aeruginosa to three clinically relevant antibiotics, we have generated a catalogue of genes that can contribute to resistance in vitro. We show that many (but not all) of these genes are clinically relevant, by identifying variants in clinical isolates of P. aeruginosa. This research furthers our understanding of the genetics leading to resistance in P. aeruginosa and provides tangible evidence that these genes can play a role clinically, potentially leading to new druggable targets or inform therapies.

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“…LGT is an important evolutionary force in prokaryotes, with up to 60% of genes within a species pangenome being acquired in this manner (Freschi et al 2018). The genes transferred can have a dramatic effect on adaptation, facilitating the colonisation of new niches and the development of novel phenotypes, as exemplified by the rapid spread of antibiotic resistance in bacteria (Ochman et al 2000).…”

Section: Introductionmentioning

confidence: 99%

Widespread lateral gene transfer among grasses

Hibdige

Raimondeau

Christin

et al. 2020

Preprint

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Background:Lateral gene transfer (LGT) has been documented in a broad range of eukaryotes, where it can promote adaptation. In plants, LGT of functional nuclear genes has been repeatedly reported in parasitic plants, ferns and grasses, but the exact extent of the phenomenon remains unknown.Systematic studies are now needed to identify the factors that govern the frequency of LGT among plants. Results:Here we scan the genomes of a diverse set of grass species that span more than 50 million years of divergence and include major crops. We identify protein coding LGT in a majority of them (13 out of 17). There is variation among species in the amount of LGT received, with rhizomatous species receiving more genes. In addition, the amount of LGT increases with phylogenetic relatedness, which might reflect genomic compatibility among close relatives facilitating successful transfers.However, we also observe genetic exchanges among distantly related species that diverged shortly after the origin of the grass family when they co-occur in the wild, pointing to a role of biogeography. The dynamics of successful LGT in grasses therefore appear to be dependent on both opportunity (co-occurrence and rhizomes) and compatibility (phylogenetic distance). Conclusion:Overall, we show that LGT is a widespread phenomenon in grasses, which is boosted by repeated contact among related lineages. The process has moved functional genes across the entire grass family into domesticated and wild species alike.LGT among them. The sampled species belong to five different clades of grasses, two from the BOP clade (Oryzoideae and Pooideae) and three from the PACMAD clade (Andropogoneae, Chloridoideae, and Paniceae). Together, these five groups capture more than 8,000 species or 70.5% of the diversity within the whole family (Soreng et al. 2015). In our sampling, each of these five groups is represented by at least two species, allowing us to monitor the number of transfers among each group. In addition, the species represent a variety of domestication status, life-history strategies, genome sizes, and ploidy levels ( Table 1). Using this sampling design, we (i) test whether LGT is more common in certain taxonomic groups, and (ii) test whether some plant characters are associated with a statistical increase of LGT. We then focus on the donors of the LGT received by the Paniceae tribe, a group for which seven genomes are available, to (iii) test whether the number of LGT increases with phylogenetic relatedness. Our work represents the first systematic quantification of LGT among members of a large group of plants and sheds new light on the conditions that promote genetic exchanges across species boundaries in plants. 94 95We modified the approach previously used by Dunning et al. (2019) to identify grass-to-grass LGT.

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ThePseudomonas aeruginosaPan-Genome Provides New Insights on Its Population Structure, Horizontal Gene Transfer, and Pathogenicity

Cited by 246 publications

References 44 publications

Gene loss and acquisition in lineages of bacteria evolving in a human host environment

Gene loss and acquisition in lineages of bacteria evolving in a human host environment

A large-scale comparison shows that genetic changes causing antibiotic resistance in experimentally evolvedPseudomonas aeruginosapredict those in naturally evolved bacteria

Widespread lateral gene transfer among grasses

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