Abstract
BackgroundMulticellular animals and bacteria frequently engage in predator-prey and host-pathogen interactions, such as the well-studied relationship between Pseudomonas aeruginosa and the nematode Caenorhabditis elegans. This study investigates the genomic and genetic basis of bacterial-driven variability in P. aeruginosa virulence towards C. elegans to provide evolutionary insights into host-pathogen relationships.ResultsNatural isolates of P. aeruginosa that exhibit diverse genomes display a broad range of virulence towards C. elegans. Using gene association and genetic analysis, we identify accessory genome elements that correlate with virulence, including both known and novel virulence determinants. Among the novel genes, we find a viral-like mobile element, the teg block, that impairs virulence and whose acquisition is restricted by CRISPR-Cas systems. Further genetic and genomic evidence suggests that spacer-targeted elements preferentially associate with lower virulence while the presence of CRISPR-Cas associates with higher virulence.ConclusionsOur analysis demonstrates substantial strain variation in P. aeruginosa virulence, mediated by specific accessory genome elements that promote increased or decreased virulence. We exemplify that viral-like accessory genome elements that decrease virulence can be restricted by bacterial CRISPR-Cas immune defense systems, and suggest a positive, albeit indirect, role for host CRISPR-Cas systems in virulence maintenance.
Highlights
Multicellular animals and bacteria frequently engage in predator-prey and host-pathogen interactions, such as the well-studied relationship between Pseudomonas aeruginosa and the nematode Caenorhabditis elegans
We addressed the sources and genomic correlates of bacteria-driven variability in the virulence of distinct P. aeruginosa strains towards C. elegans
A large P. aeruginosa accessory genome underlies substantial strain diversity in gene content To assess the extent of variation in genetic makeup among a diverse panel of environmental and clinical P. aeruginosa strains, we analyzed in silico the genomes of 1488 P. aeruginosa strains
Summary
Multicellular animals and bacteria frequently engage in predator-prey and host-pathogen interactions, such as the well-studied relationship between Pseudomonas aeruginosa and the nematode Caenorhabditis elegans. Interactions between environmental bacteria and small invertebrate animals, such as free-living nematodes, are ecologically significant in many terrestrial ecosystems [1]. These interactions comprise many types of ecological relationships that range from reciprocal harm to mutualism. Animal-bacterial interactions are “predatorprey” relationships, where for example nematodes feed on bacteria. Such predation can in turn drive the evolution of bacterial anti-predator mechanisms, such as the production of noxious toxins, and/or full pathogenic potential. C. elegans larval development can proceed successfully on P. aeruginosa, adults can suffer dramatically reduced lifetimes, depending on the P. aeruginosa strain (for example, median adult survival of ~ 2 days on strain PA14 compared to ~ 14 days on Escherichia coli strain OP50 that is used as the standard laboratory diet for Vasquez-Rifo et al Genome Biology (2019) 20:270
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