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Published on: February 23, 2014
A locus contained within a variable region of pneumococcal pathogenicity island 1 contributes to virulence in mice
Jeremy S Brown1, Sarah M Gilliland, Brian G Spratt
1Centre for Respiratory Research, Department of Medicine, Rayne Institute, Royal Free and University College Medical School, London WC1E 6JJ, United Kingdom. jeremy.brown@ucl.ac.uk
Abstract:
We have previously described a 27-kb pathogenicity island of Streptococcus pneumoniae, termed pneumococcal pathogenicity island 1 (PPI1), which contains iron uptake locus piaABCD, required for full virulence in mice, and a further 28 previously uncharacterized genes. We have investigated one of these, Sp1051, which encodes a protein of unknown function. Disruption of Sp1051 does not affect growth in laboratory broth, serum, or blood but impairs virulence in mouse models of infection. When S. pneumoniae capsular serotypes were analyzed by PCR and Southern hybridization, it was found that 33% did not contain Sp1051. Analysis of other genes within PPI1 demonstrated that, compared to the serotype 4 genome published by The Institute for Genome Research (TIGR), the genomes of many strains contain deletions of a variable number of genes between Sp1046 and Sp1064, conforming to one of six different patterns. Amplification by PCR of this PPI1 variable region from a capsular serotype 17 strain and comparison of the sequence to TIGR serotype 4 strain sequence showed that Sp1051 is contained within an 11.3-kb segment of DNA flanked by 7-bp direct repeats within the serotype 4 strain which is not present in the serotype 17 strain. Further comparison of the sequences of this region between the three published S. pneumoniae genomes demonstrated that serotype 19F and strain R6 contain novel complements of genes not present in the serotype 4 strain. These data indicate that there is striking variation in gene content and structure of the 3' region of PPI1 among strains and that this region includes at least one virulence determinant. Gene variation within horizontally acquired DNA such as that of PPI1 may be one factor modulating differences in virulence among strains.
Insights
A novel gene, Sp1051, within the pneumococcal pathogenicity island 1 (PPI1) is crucial for Streptococcus pneumoniae virulence in mice. Gene content and structure within PPI1 exhibit significant variation among strains, impacting virulence.
Area of Science:
- Microbiology
- Genetics
- Infectious Diseases
Background:
- Streptococcus pneumoniae possesses a 27-kb pathogenicity island (PPI1) with the iron uptake locus piaABCD and 28 other genes.
- The function of many genes within PPI1, including Sp1051, remains uncharacterized.
- PPI1 is known to be essential for full virulence in mouse models.
Purpose of the Study:
- To investigate the function of the uncharacterized gene Sp1051 within PPI1.
- To analyze the structural and gene content variation of PPI1 among different Streptococcus pneumoniae strains.
- To determine the role of Sp1051 and PPI1 variation in bacterial virulence.
Main Methods:
- Gene disruption of Sp1051 in Streptococcus pneumoniae.
- Assessment of bacterial growth in vitro (broth, serum, blood).
- Evaluation of virulence in mouse models of infection.
- PCR and Southern hybridization to analyze PPI1 gene content across various capsular serotypes.
- DNA sequencing and comparative analysis of the PPI1 variable region.
Main Results:
- Disruption of Sp1051 did not affect bacterial growth in vitro but significantly impaired virulence in mouse models.
- Sp1051 was absent in 33% of analyzed Streptococcus pneumoniae serotypes.
- Significant variation in gene content and structure was observed in the 3' region of PPI1 among different strains, with deletions and novel gene complements noted.
- An 11.3-kb segment containing Sp1051, flanked by direct repeats, was found in one strain but absent in another, indicating deletion events.
Conclusions:
- Sp1051 is a virulence determinant for Streptococcus pneumoniae.
- Variations in gene content and structure within the pneumococcal pathogenicity island 1 (PPI1), particularly in its 3' region, are common among strains.
- Horizontal gene transfer and subsequent variation within horizontally acquired DNA like PPI1 likely contribute to differences in strain virulence.
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