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Articles

Tolerance of a Phage Element by Streptococcus pneumoniae Leads to a Fitness Defect during Colonization

Hilary K. DeBardeleben, Elena S. Lysenko, Ankur B. Dalia, Jeffrey N. Weiser
Hilary K. DeBardeleben
aDepartment of Microbiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA
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Elena S. Lysenko
aDepartment of Microbiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA
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Ankur B. Dalia
cDepartment of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, Massachusetts, USA
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Jeffrey N. Weiser
aDepartment of Microbiology, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA
bDepartment of Pediatrics, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania, USA
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DOI: 10.1128/JB.01556-14
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ABSTRACT

The pathogenesis of the disease caused by Streptococcus pneumoniae begins with colonization of the upper respiratory tract. Temperate phages have been identified in the genomes of up to 70% of clinical isolates. How these phages affect the bacterial host during colonization is unknown. Here, we examined a clinical isolate that carries a novel prophage element, designated Spn1, which was detected in both integrated and episomal forms. Surprisingly, both lytic and lysogenic Spn1 genes were expressed under routine growth conditions. Using a mouse model of asymptomatic colonization, we demonstrate that the Spn1− strain outcompeted the Spn1+ strain >70-fold. To determine if Spn1 causes a fitness defect through a trans-acting factor, we constructed an Spn1+ mutant that does not become an episome or express phage genes. This mutant competed equally with the Spn1− strain, indicating that expression of phage genes or phage lytic activity is required to confer this fitness defect. In vitro, we demonstrate that the presence of Spn1 correlated with a defect in LytA-mediated autolysis. Furthermore, the Spn1+ strain displayed increased chain length and resistance to lysis by penicillin compared to the Spn− strain, indicating that Spn1 alters the cell wall physiology of its host strain. We posit that these changes in cell wall physiology allow for tolerance of phage gene products and are responsible for the relative defect of the Spn1+ strain during colonization. This study provides new insight into how bacteria and prophages interact and affect bacterial fitness in vivo.

FOOTNOTES

    • Received 10 February 2014.
    • Accepted 5 May 2014.
    • Accepted manuscript posted online 9 May 2014.
  • Address correspondence to Jeffrey N. Weiser, weiser{at}mail.med.upenn.edu.
  • Copyright © 2014, American Society for Microbiology. All Rights Reserved.
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Tolerance of a Phage Element by Streptococcus pneumoniae Leads to a Fitness Defect during Colonization
Hilary K. DeBardeleben, Elena S. Lysenko, Ankur B. Dalia, Jeffrey N. Weiser
Journal of Bacteriology Jun 2014, 196 (14) 2670-2680; DOI: 10.1128/JB.01556-14

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Tolerance of a Phage Element by Streptococcus pneumoniae Leads to a Fitness Defect during Colonization
Hilary K. DeBardeleben, Elena S. Lysenko, Ankur B. Dalia, Jeffrey N. Weiser
Journal of Bacteriology Jun 2014, 196 (14) 2670-2680; DOI: 10.1128/JB.01556-14
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