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Research Article | Spotlight

Intercellular Communication via the comX-Inducing Peptide (XIP) of Streptococcus mutans

Justin Kaspar, Simon A. M. Underhill, Robert C. Shields, Adrian Reyes, Suzanne Rosenzweig, Stephen J. Hagen, Robert A. Burne
George O'Toole, Editor
Justin Kaspar
aDepartment of Oral Biology, University of Florida, Gainesville, Florida, USA
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Simon A. M. Underhill
bDepartment of Physics, University of Florida, Gainesville, Florida, USA
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Robert C. Shields
aDepartment of Oral Biology, University of Florida, Gainesville, Florida, USA
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Adrian Reyes
aDepartment of Oral Biology, University of Florida, Gainesville, Florida, USA
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Suzanne Rosenzweig
bDepartment of Physics, University of Florida, Gainesville, Florida, USA
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Stephen J. Hagen
bDepartment of Physics, University of Florida, Gainesville, Florida, USA
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Robert A. Burne
aDepartment of Oral Biology, University of Florida, Gainesville, Florida, USA
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George O'Toole
Geisel School of Medicine at Dartmouth
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DOI: 10.1128/JB.00404-17
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ABSTRACT

Gram-positive bacteria utilize exported peptides to coordinate genetic and physiological processes required for biofilm formation, stress responses, and ecological competitiveness. One example is activation of natural genetic competence by ComR and the comX-inducing peptide (XIP) in Streptococcus mutans. Although the competence pathway can be activated by the addition of synthetic XIP in defined medium, the hypothesis that XIP is able to function as an intercellular signaling molecule has not been rigorously tested. Coculture model systems were developed that included a “sender” strain that overexpressed the XIP precursor (ComS) and a “responder” strain harboring a green fluorescent protein (GFP) reporter fused to a ComR-activated gene (comX) promoter. The ability of the sender strain to provide a signal to activate GFP expression was monitored at the individual cell and population levels using (i) planktonic culture systems, (ii) cells suspended in an agarose matrix, or (iii) cells growing in biofilms. XIP was shown to be freely diffusible, and XIP signaling between the S. mutans sender and responder strains did not require cell-to-cell contact. The presence of a sucrose-derived exopolysaccharide matrix diminished the efficiency of XIP signaling in biofilms, possibly by affecting the spatial distribution of XIP senders and potential responders. Intercellular signaling was greatly impaired in a strain lacking the primary autolysin, AtlA, and was substantially greater when the sender strain underwent lysis. Collectively, these data provide evidence that S. mutans XIP can indeed function as a peptide signal between cells and highlight the importance of studying signaling with an endogenously produced peptide(s) in populations in various environments and physiologic states.

IMPORTANCE The comX-inducing peptide (XIP) of Streptococcus mutans is a key regulatory element in the activation of genetic competence, which allows cells to take up extracellular DNA. XIP has been found in cell culture fluids, and the addition of synthetic XIP to physiologically receptive cells can robustly induce competence gene expression. However, there is a lack of consensus as to whether XIP can function as an intercellular communication signal. Here, we show that XIP indeed signals between cells in S. mutans, but that cell lysis may be a critical factor, as opposed to a dedicated secretion/processing system, in allowing for release of XIP into the environment. The results have important implications in the context of the ecology, virulence, and evolution of a ubiquitous human pathogen and related organisms.

FOOTNOTES

    • Received 21 June 2017.
    • Accepted 8 August 2017.
    • Accepted manuscript posted online 14 August 2017.
  • Supplemental material for this article may be found at https://doi.org/10.1128/JB.00404-17 .

  • Copyright © 2017 American Society for Microbiology.

All Rights Reserved .

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Intercellular Communication via the comX-Inducing Peptide (XIP) of Streptococcus mutans
Justin Kaspar, Simon A. M. Underhill, Robert C. Shields, Adrian Reyes, Suzanne Rosenzweig, Stephen J. Hagen, Robert A. Burne
Journal of Bacteriology Oct 2017, 199 (21) e00404-17; DOI: 10.1128/JB.00404-17

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Intercellular Communication via the comX-Inducing Peptide (XIP) of Streptococcus mutans
Justin Kaspar, Simon A. M. Underhill, Robert C. Shields, Adrian Reyes, Suzanne Rosenzweig, Stephen J. Hagen, Robert A. Burne
Journal of Bacteriology Oct 2017, 199 (21) e00404-17; DOI: 10.1128/JB.00404-17
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KEYWORDS

dental caries
genetic competence
biofilms
ComX/SigX
stress response

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