Increased mutability of Pseudomonas aeruginosa in biofilms

Driffield, Kiersten L.; Miller, Keith; Bostock, Julieanne M.; O’Neill, Alex J.; Chopra, Ian

doi:10.1093/jac/dkn044

Cited by 191 publications

(144 citation statements)

References 24 publications

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“…Excluding the 1973 isolates from the calculation, we find the mutation rate to be 6.9 × 10 −11 SNPs/bp per generation. It is important to note that these estimates show no indication of increased rates of mutation, as has been suggested for biofilm-associated cells and CF infection-associated cells due to oxidative stress or other phenomena (28)(29)(30)(31)(32).…”

Section: Resultsmentioning

confidence: 79%

Evolutionary dynamics of bacteria in a human host environment

Yang

Jelsbak

Marvig

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

313

397

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Laboratory evolution experiments have led to important findings relating organism adaptation and genomic evolution. However, continuous monitoring of long-term evolution has been lacking for natural systems, limiting our understanding of these processes in situ. Here we characterize the evolutionary dynamics of a lineage of a clinically important opportunistic bacterial pathogen, Pseudomonas aeruginosa , as it adapts to the airways of several individual cystic fibrosis patients over 200,000 bacterial generations, and provide estimates of mutation rates of bacteria in a natural environment. In contrast to predictions based on in vitro evolution experiments, we document limited diversification of the evolving lineage despite a highly structured and complex host environment. Notably, the lineage went through an initial period of rapid adaptation caused by a small number of mutations with pleiotropic effects, followed by a period of genetic drift with limited phenotypic change and a genomic signature of negative selection, suggesting that the evolving lineage has reached a major adaptive peak in the fitness landscape. This contrasts with previous findings of continued positive selection from long-term in vitro evolution experiments. The evolved phenotype of the infecting bacteria further suggests that the opportunistic pathogen has transitioned to become a primary pathogen for cystic fibrosis patients.

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Section: Resultsmentioning

confidence: 79%

Evolutionary dynamics of bacteria in a human host environment

Yang

Jelsbak

Marvig

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

313

397

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“…lower in mixed biofilms with respect to monospecific biofilms (Supplementary Figure S6). Driffield et al (2008) observed that the expression of KatA, AhpC and PA3529 were reduced in biofilms, and the frequency of ciprofloxacin-resistant mutants was increased in sessile cells with respect to planktonic cells. These authors suggested that the downregulation of antioxidant enzymes in P. aeruginosa biofilms may enhance the rate of mutagenic events owing to accumulation of DNA damage.…”

Section: Drug-resistance Proteins and Other Outer Membrane Proteins Amentioning

confidence: 95%

Interspecies competition triggers virulence and mutability in Candida albicans–Pseudomonas aeruginosa mixed biofilms

et al. 2014

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Inter-kingdom and interspecies interactions are ubiquitous in nature and are important for the survival of species and ecological balance. The investigation of microbe-microbe interactions is essential for understanding the in vivo activities of commensal and pathogenic microorganisms. Candida albicans, a polymorphic fungus, and Pseudomonas aeruginosa, a Gram-negative bacterium, are two opportunistic pathogens that interact in various polymicrobial infections in humans. To determine how P. aeruginosa affects the physiology of C. albicans and vice versa, we compared the proteomes of each species in mixed biofilms versus single-species biofilms. In addition, extracellular proteins were analyzed. We observed that, in mixed biofilms, both species showed differential expression of virulence proteins, multidrug resistance-associated proteins, proteases and cell defense, stress and iron-regulated proteins. Furthermore, in mixed biofilms, both species displayed an increase in mutability compared with monospecific biofilms. This characteristic was correlated with the downregulation of enzymes conferring protection against DNA oxidation. In mixed biofilms, P. aeruginosa regulates its production of various molecules involved in quorum sensing and induces the production of virulence factors (pyoverdine, rhamnolipids and pyocyanin), which are major contributors to the ability of this bacterium to cause disease. Overall, our results indicate that interspecies competition between these opportunistic pathogens enhances the production of virulence factors and increases mutability and thus can alter the course of hostpathogen interactions in polymicrobial infections.

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“…Further investigation into these elements would be 557 required. 558 559 Mutation frequency is known to be elevated in biofilms 34,35 , which is a measure of the 560 abundance of mutants within a population. However, mutation frequency can be 561 distorted by the expansion of lineages harbouring low probability, "jackpot mutations" 562 that occur during the early stages of growth.…”

Section: Aureus 531 532mentioning

confidence: 99%

Increased rates of genomic mutation in a biofilm co-culture model of Pseudomonas aeruginosa and Staphylococcus aureus

Frapwell

Howlin

Soren

et al. 2018

Preprint

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25Biofilms are major contributors to disease chronicity and are typically multi-species in 26 nature. Pseudomonas aeruginosa and Staphylococcus aureus are leading causes of 27 morbidity and mortality in a variety of chronic diseases but current in vitro dual-28 species biofilms models involving these pathogens are limited by short co-culture 29 times (24 to 48 hours). Here, we describe the establishment of a stable (240 hour) 30co-culture biofilm model of P. aeruginosa and S. aureus that is reproducible and 31 more representative of chronic disease. 32 33The ability of two P. aeruginosa strains, (PAO1 and a cystic fibrosis isolate, PA21), 34 to form co-culture biofilms with S. aureus was investigated. Co-culture was stable for 35 longer periods using P. aeruginosa PA21 and S. aureus viability within the model 36 improved in the presence of exogenous hemin. Biofilm co-culture was associated 37 with increased tolerance of P. aeruginosa to tobramycin and increased susceptibility 38 of S. aureus to tobramycin and a novel antimicrobial, HT61, previously shown to be 39 more effective against non-dividing cultures of Staphylococcal spp. Biofilm growth 40 was also associated with increased short-term mutation rates; 10-fold for P. (which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.

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Increased mutability of Pseudomonas aeruginosa in biofilms

Cited by 191 publications

References 24 publications

Evolutionary dynamics of bacteria in a human host environment

Evolutionary dynamics of bacteria in a human host environment

Interspecies competition triggers virulence and mutability in Candida albicans–Pseudomonas aeruginosa mixed biofilms

Increased rates of genomic mutation in a biofilm co-culture model of Pseudomonas aeruginosa and Staphylococcus aureus

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