<i>Pseudomonas aeruginosa</i> is capable of natural transformation in biofilms

Nolan, Laura M.; Turnbull, Lynne; Katrib, Marilyn; Osvath, Sarah R.; Losa, Davide; Whitchurch, Cynthia B.

doi:10.1101/859553

Cited by 6 publications

(7 citation statements)

References 35 publications

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“…The absence of surface motility of the pilU mutant observed here for A. baumannii phenocopies that of P. aeruginosa (64). Despite this commonality between the two organisms, a recent study by Nolan et al demonstrated that TFP were dispensable for low levels of natural transformation of P. aeruginosa (28), which on February 1, 2021 by guest http://jb.asm.org/ Downloaded from contrasted our findings. Here, we demonstrated that apart from PilU, the pilus components were essential for A. baumannii's natural transformability (Fig.…”

Section: Pilus Mutants Are Impaired In Their Surface Motilitycontrasting

confidence: 87%

Pilus Production in Acinetobacter baumannii Is Growth Phase Dependent and Essential for Natural Transformation

Vesel

Blokesch

2021

J Bacteriol

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Acinetobacter baumannii is a severe threat to human health as a frequently multidrug-resistant hospital-acquired pathogen. Part of the danger from this bacterium comes from its genome plasticity and ability to evolve quickly by taking up and recombining external DNA into its own genome in a process called natural competence for transformation. This mode of horizontal gene transfer is one of the major ways pathogens can acquire new antimicrobial resistances and toxic traits. Because these processes in A. baumannii are not well studied, we herein characterized new aspects of natural transformability in this species that include the species’ competence window. We uncovered a strong correlation with a growth–phase-dependent synthesis of a type IV pilus (TFP), which constitutes the central part of competence-induced DNA-uptake machinery. We used bacterial genetics and microscopy to demonstrate that the TFP is essential for the natural transformability and surface motility of A. baumannii, whereas pilus-unrelated proteins of the DNA-uptake complex do not impact the motility phenotype. Furthermore, TFP biogenesis and assembly is subject to input from two regulatory systems that are homologous to Pseudomonas aeruginosa, namely the PilSR two-component system and the Pil-Chp chemosensory system. We demonstrated that these systems not only impact the piliation status of cells but also their ability to take up DNA for transformation. Importantly, we report on discrepancies between TFP biogenesis and natural transformability within the same genus by comparing A. baumannii to data reported for A. baylyi, the latter of which served for decades as a model for natural competence. IMPORTANCE Rapid bacterial evolution has alarming negative impacts on animal and human health, which can occur when pathogens acquire antimicrobial resistance traits. As a major cause of antibiotic-resistant opportunistic infections, A. baumannii is a high priority health threat, which has motivated renewed interest in studying how this pathogen acquires new, dangerous traits. In this study, we deciphered a specific time window in which these bacteria can acquire new DNA, and correlated that with its ability to produce the external appendages that contribute to the DNA acquisition process. These cell appendages function doubly for motility on surfaces and for DNA uptake. Collectively, we showed that A. baumannii is similar in its TFP production to Pseudomonas aeruginosa, though differs from the well-studied species A. baylyi.

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Section: Pilus Mutants Are Impaired In Their Surface Motilitycontrasting

confidence: 87%

Pilus Production in Acinetobacter baumannii Is Growth Phase Dependent and Essential for Natural Transformation

Vesel

Blokesch

2021

J Bacteriol

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“…In Neisseria gonorrhoeae, genomic DNA is actively secreted through a Type 4 Secretion System by the donor strain delivering a more potent substrate of transformation than DNA released upon autolysis (51,52). In Pseudomonas aeruginosa, DNA release is dependent on a cryptic prophage endolysin that is required from biofilm formation where transformation can also occur (53)(54)(55). We found that DNA concentration in the culture supernatant of A. baumannii strain 40288 was about 2 ng/µL and a potent substrate for transformation, a result consistent with concentration measured in P. aeruginosa strain PAO1 culture (56).…”

Section: Discussionmentioning

confidence: 99%

Interbacterial transfer of carbapenem resistance and large antibiotic resistance islands by natural transformation in pathogenic Acinetobacter

Godeux

Svedholm

Barreto

et al. 2021

Preprint

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Acinetobacter baumannii infection poses a major health threat with recurrent treatment failure due to antibiotic resistance, notably to carbapenems. While genomic analyses of clinical strains indicate that homologous recombination plays a major role in the acquisition of antibiotic resistance genes, the underlying mechanisms of horizontal gene transfer often remain speculative. Our understanding of the acquisition of antibiotic resistance is hampered by the lack of experimental systems able to reproduce genomic observations. We here report the detection of recombination events occurring spontaneously in mixed bacterial populations and which can result in the acquisition of resistance to carbapenems. We show that natural transformation is the main driver of intra-, but also inter-strain recombination events between A. baumannii clinical isolates and pathogenic species of Acinetobacter. We observed that interbacterial natural transformation in mixed populations is more efficient at promoting the acquisition of large resistance islands (AbaR4, AbaR1) than providing the same bacteria with high quantities of purified genomic DNA. Importantly, analysis of the genomes of the recombinant progeny revealed large recombination tracts (from 13 to 123 kb) similar to those observed in the genome of clinical isolates. Moreover, we highlight that transforming DNA availability is a key determinant of the rate of recombination and results from both spontaneous release and interbacterial predatory behavior. Natural transformation should be considered as a leading mechanism of genome recombination and horizontal gene transfer of antibiotic resistance genes in Acinetobacter baumannii.ImportanceAcinetobacter baumannii is a multidrug resistant pathogen responsible for difficult-to-treat hospital-acquired infections. Understanding the mechanisms leading to the emergence of the multi-drug resistance in this pathogen is today crucial. Horizontal gene transfer is assumed to largely contribute to this multidrug resistance. However, in A. baumannii, the mechanisms leading to genome recombination and the horizontal transfer of resistance genes are poorly understood. We bring experimental evidence that natural transformation, a horizontal gene transfer mechanism recently highlighted in A. baumannii, allows the efficient interbacterial transfer of genetic elements carrying resistance to last line antibiotic carbapenems. Importantly, we demonstrated that natural transformation, occurring in mixed populations of Acinetobacter, enables the transfer of large resistance island mobilizing multiple resistance genes.

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“…Finally, transformation is defined as the uptake of exogenous DNA from the extracellular milieu. P. aeruginosa was initially considered incapable of natural transformation; however, recent work showed that it could take up environmental DNA, particularly when growing as a biofilm 27,28 . Transformation is harder to trace than conjugation and transduction, making it difficult to quantify its clinical impact.…”

Section: Pathways To P Aeruginosa Antibiotic Resistancementioning

confidence: 99%

How to kill Pseudomonas—emerging therapies for a challenging pathogen

Yaeger

Coles

Chan

et al. 2021

Annals of the New York Academy of Sciences

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As the number of effective antibiotics dwindled, antibiotic resistance (AR) became a pressing concern. Some Pseudomonas aeruginosa isolates are resistant to all available antibiotics. In this review, we identify the mechanisms that P. aeruginosa uses to evade antibiotics, including intrinsic, acquired, and adaptive resistance. Our review summarizes many different approaches to overcome resistance. Antimicrobial peptides have potential as therapeutics with low levels of resistance evolution. Rationally designed bacteriophage therapy can circumvent and direct evolution of AR and virulence. Vaccines and monoclonal antibodies are highlighted as immune-based treatments targeting specific P. aeruginosa antigens. This review also identifies promising drug combinations, antivirulence therapies, and considerations for new antipseudomonal discovery. Finally, we provide an update on the clinical pipeline for antipseudomonal therapies and recommend future avenues for research.

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Pseudomonas aeruginosa is capable of natural transformation in biofilms

Cited by 6 publications

References 35 publications

Pilus Production in Acinetobacter baumannii Is Growth Phase Dependent and Essential for Natural Transformation

Pilus Production in Acinetobacter baumannii Is Growth Phase Dependent and Essential for Natural Transformation

Interbacterial transfer of carbapenem resistance and large antibiotic resistance islands by natural transformation in pathogenic Acinetobacter

How to kill Pseudomonas—emerging therapies for a challenging pathogen

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