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Genetics and Molecular Biology

Expression of an Extracellular Protein (SMU.63) Is Regulated by SprV in Streptococcus mutans

Satya Deo Pandey, Indranil Biswas
Robert M. Kelly, Editor
Satya Deo Pandey
aDepartment of Microbiology, Molecular Genetics and Immunology, University of Kansas Medical Center, Kansas City, Kansas, USA
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Indranil Biswas
aDepartment of Microbiology, Molecular Genetics and Immunology, University of Kansas Medical Center, Kansas City, Kansas, USA
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  • ORCID record for Indranil Biswas
Robert M. Kelly
North Carolina State University
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DOI: 10.1128/AEM.01647-20
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ABSTRACT

In Streptococcus mutans, SprV (SMU.2137) is a pleiotropic regulator that differentially regulates genes related to competence, mutacin production, biofilm formation, and the stress tolerance response, along with some other pathways. In this study, we established a link between SprV and an ∼67-kDa protein in the culture supernatant of strain UA159 that was later confirmed as SMU.63 by matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS) analysis. We discovered that SprV downregulates the transcription and translation of SMU.63. We found that the seven amino acids from the C-terminal region of SprV were also crucial for the expression of SMU.63. Deletion of smu.63 led to increased sucrose-independent biofilm formation and competence. The sprV deletion also increased biofilm formation although this could be partially attributed to the downregulation of smu.63. In an smu.63 sprV double mutant, a synergistic effect was observed in biofilm formation in contrast to effects on competence development. We found that low or excess magnesium ion repressed sprV transcription that, in turn, affected the expression of smu.63. As expected, a magnesium ion-dependent effect of competence and biofilm formation was observed in the UA159 strain. We also replicated the results of SMU.63 expression and competence in S. mutans GS5 that encodes both SprV and SMU.63 homologs and found that the GS5 strain behaves similarly to the UA159 strain, indicating that SprV’s effect is strain independent.

IMPORTANCE We previously identified a pleiotropic regulator, SprV, in Streptococcus mutans. This regulator appears to be highly conserved among streptococci. Here, we showed that SprV regulates the expression of a secreted protein encoded by SMU.63 in S. mutans. SMU.63 has been known to impact biofilm formation and genetic competence, two important characteristics that help in colonization of the organism. SMU.63 is also unique since it is known to form amyloid fiber. We found that SprV regulates the expression of SMU.63 at both the transcriptional and translational levels. We also found that the expression of SprV is regulated by magnesium ion concentration. Interestingly, both low and high magnesium ion concentrations affected biofilm formation and genetic competence. Since SMU.63 is also highly conserved among streptococci, we hypothesized that SprV will have a similar effect on its expression.

FOOTNOTES

    • Received 7 July 2020.
    • Accepted 20 September 2020.
    • Accepted manuscript posted online 25 September 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

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Expression of an Extracellular Protein (SMU.63) Is Regulated by SprV in Streptococcus mutans
Satya Deo Pandey, Indranil Biswas
Applied and Environmental Microbiology Nov 2020, 86 (24) e01647-20; DOI: 10.1128/AEM.01647-20

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Expression of an Extracellular Protein (SMU.63) Is Regulated by SprV in Streptococcus mutans
Satya Deo Pandey, Indranil Biswas
Applied and Environmental Microbiology Nov 2020, 86 (24) e01647-20; DOI: 10.1128/AEM.01647-20
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KEYWORDS

amyloid fiber
oral streptococci
secreted protein
SprV
Streptococcus mutans
SMU.63

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