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Three paralogous LysR-type transcriptional regulators control sulfur amino acid supply in Streptococcus mutans.

ABSTRACT: The genome of Streptococcus mutans encodes 4 LysR-type transcriptional regulators (LTTRs), three of which, MetR, CysR (cysteine synthesis regulator), and HomR (homocysteine synthesis regulator), are phylogenetically related. MetR was previously shown to control methionine metabolic gene expression. Functional analysis of CysR and HomR was carried out by phenotypical studies and transcriptional analysis. CysR is required to activate the transcription of cysK encoding the cysteine biosynthesis enzyme, tcyABC and gshT genes encoding cysteine and glutathione transporter systems, and homR. HomR activates the transcription of metBC encoding methionine biosynthesis enzymes, tcyDEFGH involved in cysteine transport, and still uncharacterized thiosulfate assimilation genes. Control of HomR by CysR provides evidence of a cascade regulation for sulfur amino acid metabolism in S. mutans. Two conserved motifs were found in the promoter regions of CysR and HomR target genes, suggesting their role in the regulator binding recognition site. Both CysR and HomR require O-acetylserine to activate transcription. A global sulfur amino acid supply gene regulatory pathway is proposed for S. mutans, including the cascade regulation consequent to transcriptional activation of HomR by CysR. Phylogenetic study of MetR, CysR, and HomR homologues and comparison of their potential regulatory patterns among the Streptococcaceae suggest their rapid evolution.

SUBMITTER: Sperandio B

PROVIDER: S-EPMC2897675 | biostudies-literature | 2010 Jul

REPOSITORIES: biostudies-literature

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Three paralogous LysR-type transcriptional regulators control sulfur amino acid supply in Streptococcus mutans.

Sperandio Brice B Gautier Céline C Pons Nicolas N Ehrlich Dusko S DS Renault Pierre P Guédon Eric E

Journal of bacteriology 20100423 13

The genome of Streptococcus mutans encodes 4 LysR-type transcriptional regulators (LTTRs), three of which, MetR, CysR (cysteine synthesis regulator), and HomR (homocysteine synthesis regulator), are phylogenetically related. MetR was previously shown to control methionine metabolic gene expression. Functional analysis of CysR and HomR was carried out by phenotypical studies and transcriptional analysis. CysR is required to activate the transcription of cysK encoding the cysteine biosynthesis enz ...[more]

PMID: 20418399

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Project description:Amino sugars, particularly glucosamine (GlcN) and N-acetylglucosamine (GlcNAc), are abundant carbon and nitrogen sources supplied in host secretions and in the diet to the biofilms colonizing the human oral cavity. Evidence is emerging that these amino sugars provide ecological advantages to beneficial commensals over oral pathogens and pathobionts. Here, we performed transcriptome analysis on Streptococcus mutans and Streptococcus gordonii growing in single-species or dual-species cultures with glucose, GlcN, or GlcNAc as the primary carbohydrate source. Compared to glucose, GlcN caused drastic transcriptomic shifts in each species of bacteria when it was cultured alone. Likewise, cocultivation in the presence of GlcN yielded transcriptomic profiles that were dramatically different from the single-species results from GlcN-grown cells. In contrast, GlcNAc elicited only minor changes in the transcriptome of either organism in single- and dual-species cultures. Interestingly, genes involved in pyruvate metabolism were among the most significantly affected by GlcN in both species, and these changes were consistent with measurements of pyruvate in culture supernatants. Differing from what was found in a previous report, growth of S. mutans alone with GlcN inhibited the expression of multiple operons required for mutacin production. Cocultivation with S. gordonii consistently increased the expression of two manganese transporter operons (slo and mntH) and decreased expression of mutacin genes in S. mutans Conversely, S. gordonii appeared to be less affected by the presence of S. mutans but did show increases in genes for biosynthetic processes in the cocultures. In conclusion, amino sugars profoundly alter the interactions between pathogenic and commensal streptococci by reprogramming central metabolism.IMPORTANCE Carbohydrate metabolism is central to the development of dental caries. A variety of sugars available to dental microorganisms influence the development of caries by affecting the physiology, ecology, and pathogenic potential of tooth biofilms. Using two well-characterized oral bacteria, one pathogen (Streptococcus mutans) and one commensal (Streptococcus gordonii), in an RNA deep-sequencing analysis, we studied the impact of two abundant amino sugars on bacterial gene expression and interspecies interactions. The results indicated large-scale remodeling of gene expression induced by GlcN in particular, affecting bacterial energy generation, acid production, protein synthesis, and release of antimicrobial molecules. Our study provides novel insights into how amino sugars modify bacterial behavior, information that will be valuable in the design of new technologies to detect and prevent oral infectious diseases.

Dataset Information

Three paralogous LysR-type transcriptional regulators control sulfur amino acid supply in Streptococcus mutans.

Publications

Three paralogous LysR-type transcriptional regulators control sulfur amino acid supply in Streptococcus mutans.

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