Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H2O2

A possible counteroffensive strategy for interspecies competition

Huichun Tong, Wei Chen, Justin Merritt, Fengxia Qi, Wenyuan Shi, Xiuzhu Dong

Research output: Contribution to journalArticle

72 Citations (Scopus)

Abstract

The oral microbial flora contains over 500 different microbial species that often interact as a means to compete for limited space and nutritional resources. Streptococcus mutans, a major caries-causing pathogen, is a species which tends to interact competitively with other species in the oral cavity, largely due to its ability to generate copious quantities of the toxic metabolite, lactic acid. However, during a recent clinical study, we discovered a novel oral streptococcal species, Streptococcus oligofermentans, whose abundance appeared to be inversely correlated with that of S. mutans within dental plaque samples and thus suggested a possible antagonistic relationship with S. mutans. In this study, we used a defined in vitro interspecies interaction assay to confirm that S. oligofermentans was indeed able to inhibit the growth of S. mutans. Interestingly, this inhibitory effect was relatively specific to S. mutans and was actually enhanced by the presence of lactic acid. Biochemical analyses revealed that S. oligofermentans inhibited the growth of S. mutans via the production of hydrogen peroxide with lactic acid as the substrate. Further genetic and molecular analysis led to the discovery of the lactate oxidase (lox) gene of S. oligofermentans as responsible for this biological activity. Consequently, the lox mutant of S. oligofermentans also showed dramatically reduced inhibitory effects against S. mutans and also exhibited greatly impaired growth in the presence of the lactate produced by S. mutans. These data indicate that S. oligofermentans possesses the capacity to convert its competitor's main 'weapon' (lactic acid) into an inhibitory chemical (H2O2) in order to gain a competitive growth advantage. This fascinating ability may be an example of a counteroffensive strategy used during chemical warfare within the oral microbial community.

Original languageEnglish (US)
Pages (from-to)872-880
Number of pages9
JournalMolecular Microbiology
Volume63
Issue number3
DOIs
StatePublished - Feb 2007
Externally publishedYes

Fingerprint

Streptococcus mutans
Streptococcus
Lactic Acid
lactate 2-monooxygenase
Growth
Chemical Warfare
Dental Plaque
Weapons
Poisons
Hydrogen Peroxide
Mouth
Molecular Biology

ASJC Scopus subject areas

  • Molecular Biology
  • Microbiology

Cite this

Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H2O2 : A possible counteroffensive strategy for interspecies competition. / Tong, Huichun; Chen, Wei; Merritt, Justin; Qi, Fengxia; Shi, Wenyuan; Dong, Xiuzhu.

In: Molecular Microbiology, Vol. 63, No. 3, 02.2007, p. 872-880.

Research output: Contribution to journalArticle

@article{7896b994b42542da957dc27a3ac88805,
title = "Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H2O2: A possible counteroffensive strategy for interspecies competition",
abstract = "The oral microbial flora contains over 500 different microbial species that often interact as a means to compete for limited space and nutritional resources. Streptococcus mutans, a major caries-causing pathogen, is a species which tends to interact competitively with other species in the oral cavity, largely due to its ability to generate copious quantities of the toxic metabolite, lactic acid. However, during a recent clinical study, we discovered a novel oral streptococcal species, Streptococcus oligofermentans, whose abundance appeared to be inversely correlated with that of S. mutans within dental plaque samples and thus suggested a possible antagonistic relationship with S. mutans. In this study, we used a defined in vitro interspecies interaction assay to confirm that S. oligofermentans was indeed able to inhibit the growth of S. mutans. Interestingly, this inhibitory effect was relatively specific to S. mutans and was actually enhanced by the presence of lactic acid. Biochemical analyses revealed that S. oligofermentans inhibited the growth of S. mutans via the production of hydrogen peroxide with lactic acid as the substrate. Further genetic and molecular analysis led to the discovery of the lactate oxidase (lox) gene of S. oligofermentans as responsible for this biological activity. Consequently, the lox mutant of S. oligofermentans also showed dramatically reduced inhibitory effects against S. mutans and also exhibited greatly impaired growth in the presence of the lactate produced by S. mutans. These data indicate that S. oligofermentans possesses the capacity to convert its competitor's main 'weapon' (lactic acid) into an inhibitory chemical (H2O2) in order to gain a competitive growth advantage. This fascinating ability may be an example of a counteroffensive strategy used during chemical warfare within the oral microbial community.",
author = "Huichun Tong and Wei Chen and Justin Merritt and Fengxia Qi and Wenyuan Shi and Xiuzhu Dong",
year = "2007",
month = "2",
doi = "10.1111/j.1365-2958.2006.05546.x",
language = "English (US)",
volume = "63",
pages = "872--880",
journal = "Molecular Microbiology",
issn = "0950-382X",
publisher = "Wiley-Blackwell",
number = "3",

}

TY - JOUR

T1 - Streptococcus oligofermentans inhibits Streptococcus mutans through conversion of lactic acid into inhibitory H2O2

T2 - A possible counteroffensive strategy for interspecies competition

AU - Tong, Huichun

AU - Chen, Wei

AU - Merritt, Justin

AU - Qi, Fengxia

AU - Shi, Wenyuan

AU - Dong, Xiuzhu

PY - 2007/2

Y1 - 2007/2

N2 - The oral microbial flora contains over 500 different microbial species that often interact as a means to compete for limited space and nutritional resources. Streptococcus mutans, a major caries-causing pathogen, is a species which tends to interact competitively with other species in the oral cavity, largely due to its ability to generate copious quantities of the toxic metabolite, lactic acid. However, during a recent clinical study, we discovered a novel oral streptococcal species, Streptococcus oligofermentans, whose abundance appeared to be inversely correlated with that of S. mutans within dental plaque samples and thus suggested a possible antagonistic relationship with S. mutans. In this study, we used a defined in vitro interspecies interaction assay to confirm that S. oligofermentans was indeed able to inhibit the growth of S. mutans. Interestingly, this inhibitory effect was relatively specific to S. mutans and was actually enhanced by the presence of lactic acid. Biochemical analyses revealed that S. oligofermentans inhibited the growth of S. mutans via the production of hydrogen peroxide with lactic acid as the substrate. Further genetic and molecular analysis led to the discovery of the lactate oxidase (lox) gene of S. oligofermentans as responsible for this biological activity. Consequently, the lox mutant of S. oligofermentans also showed dramatically reduced inhibitory effects against S. mutans and also exhibited greatly impaired growth in the presence of the lactate produced by S. mutans. These data indicate that S. oligofermentans possesses the capacity to convert its competitor's main 'weapon' (lactic acid) into an inhibitory chemical (H2O2) in order to gain a competitive growth advantage. This fascinating ability may be an example of a counteroffensive strategy used during chemical warfare within the oral microbial community.

AB - The oral microbial flora contains over 500 different microbial species that often interact as a means to compete for limited space and nutritional resources. Streptococcus mutans, a major caries-causing pathogen, is a species which tends to interact competitively with other species in the oral cavity, largely due to its ability to generate copious quantities of the toxic metabolite, lactic acid. However, during a recent clinical study, we discovered a novel oral streptococcal species, Streptococcus oligofermentans, whose abundance appeared to be inversely correlated with that of S. mutans within dental plaque samples and thus suggested a possible antagonistic relationship with S. mutans. In this study, we used a defined in vitro interspecies interaction assay to confirm that S. oligofermentans was indeed able to inhibit the growth of S. mutans. Interestingly, this inhibitory effect was relatively specific to S. mutans and was actually enhanced by the presence of lactic acid. Biochemical analyses revealed that S. oligofermentans inhibited the growth of S. mutans via the production of hydrogen peroxide with lactic acid as the substrate. Further genetic and molecular analysis led to the discovery of the lactate oxidase (lox) gene of S. oligofermentans as responsible for this biological activity. Consequently, the lox mutant of S. oligofermentans also showed dramatically reduced inhibitory effects against S. mutans and also exhibited greatly impaired growth in the presence of the lactate produced by S. mutans. These data indicate that S. oligofermentans possesses the capacity to convert its competitor's main 'weapon' (lactic acid) into an inhibitory chemical (H2O2) in order to gain a competitive growth advantage. This fascinating ability may be an example of a counteroffensive strategy used during chemical warfare within the oral microbial community.

UR - http://www.scopus.com/inward/record.url?scp=33846245425&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33846245425&partnerID=8YFLogxK

U2 - 10.1111/j.1365-2958.2006.05546.x

DO - 10.1111/j.1365-2958.2006.05546.x

M3 - Article

VL - 63

SP - 872

EP - 880

JO - Molecular Microbiology

JF - Molecular Microbiology

SN - 0950-382X

IS - 3

ER -