Abstract
Bacteriophages (phages) infect many bacterial species, but little is known about the diversity of phages among the pneumococcus, a leading global pathogen. The objectives of this study were to determine the prevalence, diversity and molecular epidemiology of prophages (phage DNA integrated within the bacterial genome) among pneumococci isolated over the past 90 years. Nearly 500 pneumococcal genomes were investigated and RNA sequencing was used to explore prophage gene expression. We revealed that every pneumococcal genome contained prophage DNA. 286 full-length/putatively full-length pneumococcal prophages were identified, of which 163 have not previously been reported. Full-length prophages clustered into four major groups and every group dated from the 1930–40 s onward. There was limited evidence for genes shared between prophage clusters. Prophages typically integrated in one of five different sites within the pneumococcal genome. 72% of prophages possessed the virulence genes pblA and/or pblB. Individual prophages and the host pneumococcal genetic lineage were strongly associated and some prophages persisted for many decades. RNA sequencing provided clear evidence of prophage gene expression. Overall, pneumococcal prophages were highly prevalent, demonstrated a structured population, possessed genes associated with virulence, and were expressed under experimental conditions. Pneumococcal prophages are likely to play a more important role in pneumococcal biology and evolution than previously recognised.
Highlights
Bacteriophages infect many bacterial species, but little is known about the diversity of phages among the pneumococcus, a leading global pathogen
The key overall finding was that the breadth and depth of prophage sequences within pneumococcal genomes was astonishing
The second most important finding was that the pneumococcal prophage population does appear to be structured
Summary
Bacteriophages (phages) infect many bacterial species, but little is known about the diversity of phages among the pneumococcus, a leading global pathogen. Expressed prophage genes often have a phenotypic effect on the host bacterium, for example by producing a toxin that increases bacterial virulence (Vibrio cholerae and Staphylococcus aureus), enhancing bacterial adherence to platelets (Streptococcus mitis), or evading immune defences (Pseudomonas aeruginosa)[6,7,8]. Such genes may be functional even if the prophage is defective or the prophage genome is incomplete.
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