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Fothergill, J. L.

Publications and source records attributed to Fothergill, J. L..

9 recordsLinked to original sources

Engineering the Pseudomonas aeruginosa virus-isolation host viPAO1 reveals how host genetic barriers shape recoverable phage diversity

Cultured phage collections provide essential access to viral biology, but they capture only a small and biased fraction of natural phage diversity. Key barriers to diverse phage isolation are likely to include the prophages and defence systems present in the genomes of isolation hosts. Here, we show that removal of these host genetic barriers expands recoverable phage diversity in Pseudomonas aeruginosa. We constructed a series of progressively more permissive hosts derived from MPAO1 by sequentially deleting intracellular defence systems and resident prophages, culminating in viPAO1 (virus-isolation PAO1). Sequential removal of these barriers increased phage susceptibility, with Gabija and type I restriction-modification acting as major barriers to phage infection. In comparative isolation experiments, removal of intracellular barriers produced the largest increase in phage recovery, while additional receptor modification altered the composition of recovered phage subsets. viPAO1 also substantially increased recovery of phage contigs from environmental samples. Scaling this approach across 1090 clinical isolates enabled recovery of a curated collection of 69 individually purified temperate P. aeruginosa phages spanning 24 predicted genera, including 15 putative novel genera. Together, these findings demonstrate that removal of host genetic barriers to infection enhances recoverable phage diversity and establish permissive host engineering as a practical strategy for uncovering under-sampled regions of cultured phage diversity.

microbiology↗

Multiple ecological and evolutionary mechanisms drive treatment-induced antibiotic resistance

The emergence of resistance within patients during antibiotic treatment is an important cause of treatment failure. However, the ecological and evolutionary mechanisms driving within-patient emergence remain poorly understood. Here, we analysed 24,478 Pseudomonas aeruginosa isolates sampled from 180 bronchiectasis patients during a clinical trial to understand how ciprofloxacin-resistant infections emerged over a one-year period of pulse-dosing. Pre-existing resistance predominated, accelerating resistance emergence relative to patients where resistance emerged by spontaneous mutation or strain immigration. Selective sweeps of costly mutations increased resistance over time in some patients, whereas in others oscillating resistance levels were driven by antibiotic treatment and resistance-growth trade-offs between genetically divergent subpopulations. Our findings show that infections under identical treatment follow diverse and sometimes complex ecological and evolutionary paths to antibiotic resistance, with implications for better predicting and managing treatment-induced antibiotic resistance.

evolutionary biology↗

Defence systems drive accessory genome interactions in Pseudomonas aeruginosa.

Bacterial genomes represent dynamic ecological systems in which mutational selection and dynamic accessory genome element complements drive evolution. Emerging evidence suggests that bacterial defence systems, which protect against phages and other mobile genetic elements, interact through cooperative, competitive, and antagonistic relationships. These interactions can influence horizontal gene transfer, shape phage susceptibility, and the diversification of genome composition across environments. Recent ecological studies describe non-random co-occurrence and avoidance of defence systems, suggesting that they may emerge from ecological and evolutionary interactions, rather than by chance. This necessitates exploring whether these patterns reflect functional compatibility, shared selection pressures imposed by ecological niche, or if they merely arise from co-localisations of convenience. Understanding these patterns is key to elucidating how the accessory genome evolves and how defence systems constrain or facilitate genome plasticity. To investigate these patterns, in their genomic context, and provide a resource for future investigations, we analysed the distributions of defence systems and other accessory genome elements in a recently curated global dataset of 2,940 Pseudomonas aeruginosa genomes. Genomic defence system content varied by ecological niche, with higher numbers per genome in non-cystic fibrosis derived isolates (average n=7.9) compared to cystic fibrosis-derived isolates (average n=6.5). We identified multiple associations (n=426) and dissociations (n=50) among defence systems, and among other accessory genome elements, many of which had a plausible biological explanation. We also quantitated the relative interactions among accessory genome elements which revealed that defence systems and anti-defence systems engage in the most accessory genome interactions, compared with e.g. antimicrobial resistance genes, plasmids, phages, suggesting that systems are a major driving force in the ecological dynamics of the bacterial accessory genome. Together, these patterns provide new insights into the evolutionary forces shaping bacterial genomes, provide a valuable resource of quantitated interactions in a highly curated Pseudomonas aeruginosa dataset, and establish a framework for future mechanistic and ecological investigations of defence system interactions.

microbiology↗

Sputum Proteomics reveals unique signatures linked to key outcomes in cystic fibrosis trials.

RationaleLung function (FEV1) and quality of life (QoL) are key outcomes in most interventional clinical trials conducted in people living with cystic fibrosis. However, no robust pre-clinical surrogates for FEV1 and QoL exist. The precise physiological mechanisms leading to treatment-related improvements in these outcomes are incompletely understood. In this post-hoc analysis we explored the relationship between changes in the sputum proteome and these outcomes with the aim of identifying translational biomarkers. MethodsPaired sputum samples collected during the AZTEC-CF study (NCT02894684) pre and post 14 days of antibiotic treatment for an acute pulmonary exacerbation were included. Samples were analysed using in vitro Mesoscale Discovery (MSD) assays and by nano LC-MS/MS. Peptide identification and quantification was performed and the log-fold change for individual proteins and relationships between protein change and changes in FEV1 and QoL were evaluated. ResultsDistinct patterns were found between proteins that correlated with FEV1 and those that correlated with QoL improvements. FEV1 improvement was characterised by increases in bacterially-derived proteins accompanied by decreases in proteins relating to neutrophil degranulation. Conversely, changes in QoL were associated with increases in antiprotease and antioxidant proteins. MSD analysis revealed changes in some neutrophil-associated markers significantly correlated with FEV1 improvements, but no markers significantly correlated with QoL improvements. ConclusionsThese results suggest changes in two key CF clinical trial outcomes (FEV1 and QoL) may be underpinned by different physiological mechanisms. Understanding these divergent mechanisms is vital to fortify optimal clinical trial design in CF and panels of biomarkers may be needed to improve translational confidence.

immunology↗

Real-time label-free exploration of the dynamics and interactions of bacteriophages

1.Bacteriophages are the focus of extensive research and monitoring their dynamics and interactions with bacterial hosts is crucial to characterise the mechanisms of infection and support potential applications in biotechnology and medicine. Traditional monitoring techniques rely on the fluorescent labelling of bacteriophages due to their size being nanometric. In this paper, we propose a novel, label-free method to generate optical signatures of bacteriophages in a conventional microscopy setup by exploiting the optical phenomenon of caustics. We utilised previously isolated Pseudomonas aeruginosa phage (pelp20 and phiKZ) and a novel Escherichia coli phage (EcoLiv25) to demonstrate detection and tracking within liquid laboratory media. The results obtained confirm the feasibility of visualising and monitoring over time a diverse array of bacteriophages, offering a simpler and less invasive means of observation for research and application in microbiology and related fields.

microbiology↗

Global genomic diversity of Pseudomonas aeruginosa in bronchiectasis

BackgroundPseudomonas aeruginosa is the dominant pathogen causing lung infections in people with both cystic fibrosis (CF) and bronchiectasis, associated with poorer outcomes. Unlike CF, bronchiectasis has been a neglected disease. More extensive genomic studies of larger bronchiectasis patient cohorts and within patient sampling are needed to improve understanding of the evolutionary mechanisms underpinning P. aeruginosa infections to guide novel and improved treatments. MethodsWe have performed genome sequencing of 2,854 P. aeruginosa isolates from 180 patients attending clinics worldwide to analyse the genomic diversity between and within patient infections. ResultsWe observed high genetic diversity between infections with low incidence of highly transmissible strains. Our genomic data provide evidence for the mutational targets driving P. aeruginosa evolution in bronchiectasis. Some functions found to gain mutations were comparable to CF, including biofilm and iron acquisition, whilst others highlighted distinct evolutionary paths in bronchiectasis such as pyocin production and resistance, and a novel efflux pump gene (PA1874). We also show a high incidence of antimicrobial resistance-associated mutations and acquired resistance genes, in particular multidrug efflux and fluoroquinolone resistance mechanisms. ConclusionsOur findings highlight important differences between P. aeruginosa infections in bronchiectasis and CF and provide evidence of the relatively minor role transmissible strains play in bronchiectasis. Our study provides a 10-fold increase in the available genomic data for these infections and is a global resource to improve our knowledge and understanding, to facilitate better patient outcomes. SummaryThe largest genomic study of Pseudomonas aeruginosa bronchiectasis isolates to-date, providing an unprecedented global genomic resource. We highlight important differences between bronchiectasis and cystic fibrosis, including key genes under selection.

genomics↗

Optimisation of a DNA extraction protocol for improving the bacterial and fungal classification based on Nanopore sequencing

Ribosomal RNA gene amplicon sequencing is commonly used to evaluate microbiome profiles in health and disease and document the impact of interventional treatments. Long-read nanopore sequencing is attractive since it can provide greater classification at the species level. However, optimised protocols to target marker genes for bacterial and fungal profiling are needed. To achieve an increased taxonomic resolution, we developed extraction and long-amplicon PCR-based approaches using Nanopore sequencing. Three sample lysis conditions were applied to a mock microbial community, including known bacterial and fungal species; the 96 MagBead DNA lysis buffer (ML) alone, incorporating bead-beating (MLB) or bead-beating plus MetaPolyzyme enzymatic treatment (MLBE). Profiling of bacterial comparison, MLB had more statistically different bacterial phyla and genera than the others. For fungal profiling, MLB had a significant increase of Ascomycota and a decline of Basidiomycota, subsequently failing to detect Malassezia and Cryptococcus. Also, the principal coordinates analysis (PCoA) plot by the Bray-Curtis index showed a significant difference among groups for bacterial (p = 0.033) and fungal (p = 0.012) profiles. Overall, the microbial profiling and diversity analysis revealed that ML and MLBE have more similarity than MLB for both bacteria and fungi, therefore, bead-beating is not recommended for long-read amplicon sequencing. However, ML alone was suggested as an optimal approach considering DNA yield, classification, reagent cost and hands-on time. This could be an initial proof-of-concept study for simultaneous human microbiome and mycobiome studies.

microbiology↗

Pseudomonas aeruginosa utilises host-derived polyamines to facilitate antimicrobial tolerance

Pseudomonas aeruginosa undergoes diversification during infection of the cystic fibrosis (CF) lung. Understanding these changes requires model systems that capture the complexity of the CF lung environment. We previously identified loss-of-function mutations in the two-component regulatory system sensor kinase gene pmrB, in P. aeruginosa from CF and from experimental infection of mice. Here, we demonstrate that whilst such mutations lower in vitro MICs for multiple antimicrobial classes, this is not reflected in increased antibiotic susceptibility in vivo. Loss of PmrB impairs aminoarabinose modification of lipopolysaccharide, increasing the negative charge of the outer membrane and promoting uptake of cationic antimicrobials. However, in vivo, this can be offset by increased membrane binding of other positively charged molecules present in lungs. The polyamine spermidine readily coats the surface of PmrB-deficient P. aeruginosa, reducing susceptibility to antibiotics that rely on charge differences to bind the outer membrane and increasing biofilm formation. Spermidine is elevated in lungs during P. aeruginosa infection in mice and during episodes of antimicrobial treatment in people with CF. These findings highlight the need to study antimicrobial resistance under clinically relevant environmental conditions. Microbial mutations carrying fitness costs in vitro may be advantageous during infection, where host resources can be utilised.

microbiology↗

A megaplasmid family responsible for dissemination of multidrug resistance in Pseudomonas

Multidrug resistance (MDR) represents a global threat to health. Although plasmids can play an important role in the dissemination of MDR, they have not been commonly linked to the emergence of antimicrobial resistance in the pathogen Pseudomonas aeruginosa. We used whole genome sequencing to characterize a collection of P. aeruginosa clinical isolates from a hospital in Thailand. Using long-read sequence data we obtained complete sequences of two closely related megaplasmids (>420 kb) carrying large arrays of antibiotic resistance genes located in discrete, complex and dynamic resistance regions, and revealing evidence of extensive duplication and recombination events. A comprehensive pangenomic and phylogenomic analysis indicated that 1) these large plasmids comprise a family present in different members of the Pseudomonas genus and associated with multiple sources (geographical, clinical or environmental); 2) the megaplasmids encode diverse niche-adaptive accessory traits, including multidrug resistance; 3) the pangenome of the megaplasmid family is highly flexible and diverse, comprising a substantial core genome (average of 48% of plasmid genes), but with individual members carrying large numbers of unique genes. The history of the megaplasmid family, inferred from our analysis of the available database, suggests that members carrying multiple resistance genes date back to at least the 1970s.\n\nFundingThis work was supported by the International Pseudomonas Genomics Consortium, funded by Cystic Fibrosis Canada [RCL]; and the Secretaria de Educacion, Ciencia, Tecnologia e Innovacion (SECTEI), Mexico [AC].

microbiology↗