Autoinducer-2-Regulated Genes in Streptococcus mutans and Impact on Oral Bacterial Communities

Julie A. Perry; Dennis G. Cvitkovitch

doi:10.1128/9781555817107.ch17

Chapter 17 : Autoinducer-2-Regulated Genes in Streptococcus mutans and Impact on Oral Bacterial Communities

Authors: Julie A. Perry¹, Dennis G. Cvitkovitch²

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Affiliations: 1: Dental Research Institute, Faculty of Dentistry, University of Toronto, Toronto, ON Canada M5G 1G6; 2: Dental Research Institute, Faculty of Dentistry, University of Toronto, Toronto, ON Canada M5G 1G6

Content Type: Monograph

Publication Year: 2011

Category: Genomics and Bioinformatics

Book DOI: 10.1128/9781555817107

Chapter DOI: 10.1128/9781555817107.ch17

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Abstract:

This chapter explores the mechanism of interspecies cell-cell communication in the oral biofilm, with emphasis on the cariogenic organism Streptococcus mutans. Bioluminescence in the marine organism Vibrio harveyi was one of the first examples of quorum sensing behavior described to occur in nature. The gene required for autoinducer 2 (AI-2) production encodes the enzyme LuxS, which functions in the S-adenosylmethionine (SAM) utilization pathway. Biofilms are complex communities where close interactions between heterogeneous species are common. Alterations in AI-2 signaling might affect biofilm formation in several ways, and changes in the cells themselves during the physiologically distinct biofilm mode of growth might reciprocally affect AI-2 signaling. Exopolysaccharide (EPS) production occurs after attachment and is involved in the latter stages of biofilm maturation. The genetic basis for altered biofilm structure in S. mutans luxS mutants has been attributed to an overexpression of the general stress response genes encoding GroEL and DnaK or to increased glucosyltransferase expression. The majority of genes found to respond to the AI-2 signal were genes involved in protein synthesis and genes for hypothetical proteins. A convincing demonstration of S. mutans complementing a luxS deletion in another species would be helpful in establishing the true nature of this signal. Interference with AI-2-mediated signaling occurs between competing microorganisms that share the same niche.

Citation: Perry J, Cvitkovitch D. 2011. Autoinducer-2-Regulated Genes in Streptococcus mutans and Impact on Oral Bacterial Communities, p 247-261. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch17

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Autoinducer-2-Regulated Genes in Streptococcus mutans and Impact on Oral Bacterial Communities

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FIGURE 1

Schematic representation of quorum sensing systems in bacteria. (Top left) LuxI/R quorum sensing in gram-negative bacteria. AHL molecules are synthesized by a homologue of the LuxI autoinducer synthase and freely diffuse out of the cell. At a specific concentration, AHL binds a homologue of the LuxR response regulator which then activates transcription of target genes. (Bottom left) Peptide quorum sensing system of gram-positive bacteria. The quorum sensing signal is synthesized as a pre-peptide, which is processed upon export by an ABC transporter to generate the mature signal. The peptide binds to its cognate receptor protein, a histidine kinase sensor, which autophosphorylates on a conserved histidine residue. The phosphoryl group is subsequently transferred to a response regulator protein, which regulates transcription of target genes. (Top and bottom right) Quorum sensing in V. harveyi. AI-1 is synthesized by LuxLM and sensed by LuxN. LuxS synthesizes the AI-2 furanone signal, which is detected at the cell surface by the LuxP periplasmic binding protein and the receptor LuxQ. Both pathways converge at the shared LuxU phosphorelay protein, and LuxO activates transcription of target genes.

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FIGURE 1

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FIGURE 2

Simplified representation of the activated methyl cycle and production of AI-2.

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FIGURE 2

Simplified representation of the activated methyl cycle and production of AI-2.

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FIGURE 3

Schematic representation of the system developed by Yoshida et al. ( 62 ) to study diffusible signal molecules. S. mutans luxS mutants are inoculated into the culture medium (far left). A tissue culture insert, containing a filter permeative to small molecules, is placed into the well, and the insert is inoculated with a second oral microorganism (middle). Both organisms are allowed to grow in the presence of diffusible (and reciprocal) signaling molecules. At the conclusion of the experiment, the tissue culture insert is removed and the phenotypic effect of signaling is measured on the S. mutans luxS biofilm (far right).

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FIGURE 3

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FIGURE 4

Examples of chemical signaling within the oral biofilm. Solid black arrows represent signaling via AI-2, which has been shown to influence both monospecies and mixed-species biofilm formation in S. gordonii ( 4 , 30 ). AI-2 signaling has also been implicated in S. mutans monospecies biofilms ( 33 , 56 , 57 ). Soluble factors (presumed to be AI-2) produced by S. gordonii, S. sobrinus, and S. anginosus have been shown to complement the S. mutans luxS mutant biofilm phenotype ( 62 ). Besides AI-2, chemical signaling occurs between S. gordonii and Vibrio atypica to increase production of lactic acid (the preferred carbon source for V. atypica) in the former and foster a mutualistic partnership in the biofilm ( 12 ) (open arrow). Finally, S. mutans is known to regulate its competence response, stress tolerance response, and biofilm formation through its intraspecies peptide quorum sensing signal CSP (dashed arrow) ( 27 – 29 ).

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FIGURE 4

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Tables

Autoinducer-2-Regulated Genes in Streptococcus mutans and Impact on Oral Bacterial Communities

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TABLE 1

Effect of deletion of luxS on oral microorganisms

TABLE 1

Effect of deletion of luxS on oral microorganisms

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TABLE 2

Genes regulated by AI-2 signaling in S. mutans a

TABLE 2

Genes regulated by AI-2 signaling in S. mutans a