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Mechanisms of Action: Physiological Effects

Spontaneously Arising Streptococcus mutans Variants with Reduced Susceptibility to Chlorhexidine Display Genetic Defects and Diminished Fitness

Justin R. Kaspar, Matthew J. Godwin, Irina M. Velsko, Vincent P. Richards, Robert A. Burne
Justin R. Kaspar
aDepartment of Oral Biology, University of Florida, Gainesville, Florida, USA
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Matthew J. Godwin
aDepartment of Oral Biology, University of Florida, Gainesville, Florida, USA
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Irina M. Velsko
bDepartment of Biological Sciences, Clemson University, Clemson, South Carolina, USA
cMax Planck Institute for the Science of Human History, Jena, Germany
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Vincent P. Richards
bDepartment of Biological Sciences, Clemson University, Clemson, South Carolina, USA
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Robert A. Burne
aDepartment of Oral Biology, University of Florida, Gainesville, Florida, USA
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DOI: 10.1128/AAC.00161-19
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ABSTRACT

Chlorhexidine (CHX) has been used to control dental caries caused by acid-tolerant bacteria such as Streptococcus mutans since the 1970s. Repeat CHX exposure for other bacterial species results in the development of variants with reduced susceptibility that also become more resistant to other antimicrobials. It has not been tested if such variants arise when streptococci are exposed to CHX. Here, we passaged S. mutans in increasing concentrations of CHX and isolated spontaneously arising reduced susceptibility variants (RSVs) from separate lineages that have MICs that are up to 3-fold greater than the parental strain. The RSVs have increased growth rates at neutral pH and under acidic conditions in the presence of CHX but accumulate less biomass in biofilms. RSVs display higher MICs for daptomycin and clindamycin but increased sensitivity to dental-relevant antimicrobials triclosan and sodium fluoride. Plate-based assays for competition with health-associated oral streptococci revealed decreased bacteriocin production by the RSVs, increased sensitivity to hydrogen peroxide, and diminished competitive fitness in a human-derived ex vivo biofilm consortium. Whole-genome sequencing identified common single nucleotide polymorphisms (SNPs) within a diacylglycerol kinase homolog and a glycolipid synthesis enzyme, which could alter the accumulation of lipoteichoic acids and other envelope constituents, as well as a variety of mutations in other genes. Collectively, these findings confirm that S. mutans and likely other streptococci can develop tolerance to CHX but that increased tolerance comes at a fitness cost, such that CHX-induced variants that spontaneously arise in the human oral cavity may not persist.

FOOTNOTES

    • Received 6 February 2019.
    • Returned for modification 1 March 2019.
    • Accepted 20 April 2019.
    • Accepted manuscript posted online 29 April 2019.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AAC.00161-19.

  • Copyright © 2019 American Society for Microbiology.

All Rights Reserved.

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Spontaneously Arising Streptococcus mutans Variants with Reduced Susceptibility to Chlorhexidine Display Genetic Defects and Diminished Fitness
Justin R. Kaspar, Matthew J. Godwin, Irina M. Velsko, Vincent P. Richards, Robert A. Burne
Antimicrobial Agents and Chemotherapy Jun 2019, 63 (7) e00161-19; DOI: 10.1128/AAC.00161-19

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Spontaneously Arising Streptococcus mutans Variants with Reduced Susceptibility to Chlorhexidine Display Genetic Defects and Diminished Fitness
Justin R. Kaspar, Matthew J. Godwin, Irina M. Velsko, Vincent P. Richards, Robert A. Burne
Antimicrobial Agents and Chemotherapy Jun 2019, 63 (7) e00161-19; DOI: 10.1128/AAC.00161-19
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KEYWORDS

Streptococcus mutans
antimicrobial tolerance
antimicrobials
biofilms
chlorhexidine
dental caries
microbial antagonism
oral microbiome
stress response

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