Dataset Information

Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa.

ABSTRACT: Pseudomonas aeruginosa isolates have a highly conserved core genome representing up to 90% of the total genomic sequence with additional variable accessory genes, many of which are found in genomic islands or islets. The identification of the Liverpool Epidemic Strain (LES) in a children's cystic fibrosis (CF) unit in 1996 and its subsequent observation in several centers in the United Kingdom challenged the previous widespread assumption that CF patients acquire only unique strains of P. aeruginosa from the environment. To learn about the forces that shaped the development of this important epidemic strain, the genome of the earliest archived LES isolate, LESB58, was sequenced. The sequence revealed the presence of many large genomic islands, including five prophage clusters, one defective (pyocin) prophage cluster, and five non-phage islands. To determine the role of these clusters, an unbiased signature tagged mutagenesis study was performed, followed by selection in the chronic rat lung infection model. Forty-seven mutants were identified by sequencing, including mutants in several genes known to be involved in Pseudomonas infection. Furthermore, genes from four prophage clusters and one genomic island were identified and in direct competition studies with the parent isolate; four were demonstrated to strongly impact on competitiveness in the chronic rat lung infection model. This strongly indicates that enhanced in vivo competitiveness is a major driver for maintenance and diversifying selection of these genomic prophage genes.

SUBMITTER: Winstanley C

PROVIDER: S-EPMC2612960 | biostudies-literature | 2009 Jan

REPOSITORIES: biostudies-literature

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Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa.

Winstanley Craig C Langille Morgan G I MG Fothergill Joanne L JL Kukavica-Ibrulj Irena I Paradis-Bleau Catherine C Sanschagrin François F Thomson Nicholas R NR Winsor Geoff L GL Quail Michael A MA Lennard Nicola N Bignell Alexandra A Clarke Louise L Seeger Kathy K Saunders David D Harris David D Parkhill Julian J Hancock Robert E W RE Brinkman Fiona S L FS Levesque Roger C RC

Genome research 20081201 1

Pseudomonas aeruginosa isolates have a highly conserved core genome representing up to 90% of the total genomic sequence with additional variable accessory genes, many of which are found in genomic islands or islets. The identification of the Liverpool Epidemic Strain (LES) in a children's cystic fibrosis (CF) unit in 1996 and its subsequent observation in several centers in the United Kingdom challenged the previous widespread assumption that CF patients acquire only unique strains of P. aerugi ...[more]

PMID: 19047519

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Project description:Wolbachia endosymbionts can induce multiple reproductive manipulations in their hosts, with cytoplasmic incompatibility (CI) being one of the most common manipulations. Two important agricultural pests, the white-backed planthopper (Sogatella furcifera) and the brown planthopper (Nilaparvata lugens), are usually infected with CI-inducing Wolbachia strain wFur and non-CI-inducing Wolbachia strain wLug, respectively. The biological effects of these infections when present in a host cell are unknown. Here, we introduced the two Wolbachia strains into an Aedes albopictus cell line to stably establish a wFur-infected cell line (WFI) and a wLug-infected cell line (WLI). In a mixed culture, WFI cells were completely replaced by WLI cells, pointing to a stronger competitiveness of the WLI cell line. We found that infection by both Wolbachia strains reduced cell growth rates, but WLI had a higher cell growth rate than WFI, and this difference in cell growth rate combined with possible Wolbachia differences in diffusivity may have affected cell competitiveness. By examining gene expression and metabolites in the two lines, we found that some genes and key metabolites responded to differences in cell competitiveness. These results point to potential mechanisms that could contribute to the relative performance of hosts infected by these strains and also highlight the substantial impact of a non-CI Wolbachia on metabolism, which may in turn influence the fitness of its native host. IMPORTANCE Wolbachia transinfection in insects can be used to suppress pests and block virus transmission. We stably introduced two Wolbachia strains from rice planthoppers into cell lines of an important arbovirus mosquito vector, Aedes albopictus. The levels of competitiveness of host cells from the lines infected by the two Wolbachia strains were different, as were metabolic responses of the cell lines. These results suggest potential metabolic effects of Wolbachia on native hosts that could be exploited when they are transinfected into novel hosts for pest control.

Project description:Pseudomonas aeruginosa is a notorious pathogen that causes various nosocomial infections. Several prophage genes located on the chromosomes of P. aeruginosa have been reported to contribute to bacterial pathogenesis via host phenotype transformations, such as serotype conversion and antibiotic resistance. However, our understanding of the molecular mechanism behind host phenotype shifts induced by prophage genes remains largely unknown. Here, we report a systematic study around a hypothetical recombinase, Pg54 (RecT), located on a 48-kb putative prophage (designated PP9W) of a clinical P. aeruginosa strain P9W. Using a ΔrecT mutant (designated P9D), we found that RecT promoted prophage PP9W excision and gene transcription via the inhibition of the gene expression level of pg40, which encodes a CI-like repressor protein. Further transcriptomic profiling and various phenotypic tests showed that RecT modulated like a suppressor to some transcription factors and vital genes of diverse cellular processes, providing multiple advantages for the host, including cell growth, biofilm formation, and virulence. The versatile functions of RecT hint at a strong impact of phage proteins on host P. aeruginosa phenotypic flexibility. IMPORTANCE Multidrug-resistant and metabolically versatile P. aeruginosa are difficult to eradicate by anti-infective therapy and frequently lead to significant morbidity and mortality. This study characterizes a putative recombinase (RecT) encoded by a prophage of a clinical P. aeruginosa strain isolated from severely burned patients, altering prophage lifestyle and host core cellular processes. It implies the potential role of RecT in the coevolution arm race between bacteria and phage. The excised free phages from the chromosome of host bacteria can be used as weapons against other sensitive competitors in diverse environments, which may increase the lysogeny frequency of different P. aeruginosa subgroups. Subsequent analyses revealed that RecT both positively and negatively affects different phenotypic traits of the host. These findings concerning RecT functions of host phenotypic flexibility improve our understanding of the association between phage recombinases and clinical P. aeruginosa, providing new insight into mitigating the pathogen infection.

Dataset Information

Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa.

Publications

Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa.

Similar Datasets

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