Dataset Information

Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans.

ABSTRACT: The abilities of Streptococcus mutans to form biofilms and to survive acidic pH are regarded as two important virulence determinants in the pathogenesis of dental caries. Environmental stimuli are thought to regulate the expression of several genes associated with virulence factors through the activity of two-component signal transduction systems. Yet, little is known of the involvement of these systems in the physiology and pathogenicity of S. mutans. In this study, we describe a two-component regulatory system and its involvement in biofilm formation and acid resistance in S. mutans. By searching the S. mutans genome database with tblastn with the HK03 and RR03 protein sequences from S. pneumoniae as queries, we identified two genes, designated hk11 and rr11, that encode a putative histidine kinase and its cognate response regulator. To gain insight into their function, a PCR-mediated allelic-exchange mutagenesis strategy was used to create the hk11 (Em(r)) and rr11 (Em(r)) deletion mutants from S. mutans wild-type NG8 named SMHK11 and SMRR11, respectively. The mutants were examined for their growth rates, genetic competence, ability to form biofilms, and resistance to low-pH challenge. The results showed that deletion of hk11 or rr11 resulted in defects in biofilm formation and resistance to acidic pH. Both mutants formed biofilms with reduced biomass (50 to 70% of the density of the parent strain). Scanning electron microscopy revealed that the biofilms formed by the mutants had sponge-like architecture with what appeared to be large gaps that resembled water channel-like structures. The mutant biofilms were composed of longer chains of cells than those of the parent biofilm. Deletion of hk11 also resulted in greatly diminished resistance to low pH, although we did not observe the same effect when rr11 was deleted. Genetic competence was not affected in either mutant. The results suggested that the gene product of hk11 in S. mutans might act as a pH sensor that could cross talk with one or more response regulators. We conclude that the two-component signal transduction system encoded by hk11 and rr11 represents a new regulatory system involved in biofilm formation and acid resistance in S. mutans.

SUBMITTER: Li YH

PROVIDER: S-EPMC151940 | biostudies-literature | 2002 Nov

REPOSITORIES: biostudies-literature

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Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans.

Li Yung-Hua YH Lau Peter C Y PC Tang Nan N Svensäter Gunnel G Ellen Richard P RP Cvitkovitch Dennis G DG

Journal of bacteriology 20021101 22

The abilities of Streptococcus mutans to form biofilms and to survive acidic pH are regarded as two important virulence determinants in the pathogenesis of dental caries. Environmental stimuli are thought to regulate the expression of several genes associated with virulence factors through the activity of two-component signal transduction systems. Yet, little is known of the involvement of these systems in the physiology and pathogenicity of S. mutans. In this study, we describe a two-component ...[more]

PMID: 12399503

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Project description:Biofilm formation is considered the most important factor involved in pathogenicity of Staphylococcus epidermidis.We investigated the role of two-component signal transduction system (TCS) srrAB, which was up-regulated under micro-aerobic condition, in the growth and biofilm formation of S. epidermidis.AsrrA-deficient mutant (M-bM-^HM-^FsrrA) derived from S. epidermidis1457 (SE1457), exhibited dramatic reduction in growth and biofilm formation underboth aerobic and micro-aerobic conditions, and more sensitive to several different types of antimicrobial agents, H2O2 and SDS. In New Zealand Rabbit model of S. epidermidis biofilm infection, M-bM-^HM-^FsrrA hardly formed biofilm compared to that of SE1457. Phenotypic alteration was restored to the wide-type levelwhen srrAB were complemented into M-bM-^HM-^FsrrA. Further study found that the initial adherence capacity and production of polysaccharide intercellular adhesion (PIA) in M-bM-^HM-^FsrrA were decreased, while extracellular DNA (eDNA) was increased. Transcriptional Analysisby qRT-PCR demonstrated that expression level of icaRin M-bM-^HM-^FsrrA was up-regulated compared to that of SE1457 under aerobic condition, while down-regulated under micro-aerobic condition;icaA and altE were down-regulated under both conditions. Expression of genes involved in respiratory metabolism, such as qoxB(quinol oxidase polypeptide II), ctaA(heme A synthase), and pfl(pyruvate formatelyase), etc. were down-regulated in M-bM-^HM-^FsrrAunder both conditions. Electrophoretic mobility shift assay (EMSA) revealed that phosphorylated SrrA bound to the promoter regions of icaR, icaA, atlE, qoxB,ctaA, andpflB just like binding its own promoter region srr. Taken together, our results demonstrate that srrAB may provide a mechanistic link between respiratory metabolism, environmental signals, and regulation of biofilm formation in S. epidermidis. Microarrays covering different S. epidermidis genomes were used to assess the impact of the two component system srrAB on growth and biofilm formation, by comparing WT with srrA mutant transcriptomes

Project description:Efficient biofilm formation and root colonization capabilities facilitate the ability of beneficial plant rhizobacteria to promote plant growth and antagonize soilborne pathogens. Biofilm formation by plant-beneficial Bacillus strains is triggered by environmental cues, including oxygen deficiency, but the pathways that sense these environmental signals and regulate biofilm formation have not been thoroughly elucidated. In this study, we showed that the ResDE two-component regulatory system in the plant growth-promoting rhizobacterium Bacillus amyloliquefaciens strain SQR9 senses the oxygen deficiency signal and regulates biofilm formation. ResE is activated by sensing the oxygen limitation-induced reduction of the NAD+/NADH pool through its PAS domain, stimulating its kinase activity, and resulting in the transfer of a phosphoryl group to ResD. The phosphorylated ResD directly binds to the promoter regions of the qoxABCD and ctaCDEF operons to improve the biosynthesis of terminal oxidases, which can interact with KinB to activate biofilm formation. These results not only revealed the novel regulatory function of the ResDE two-component system but also contributed to the understanding of the complicated regulatory network governing Bacillus biofilm formation. This research may help to enhance the root colonization and the plant-beneficial efficiency of SQR9 and other Bacillus rhizobacteria used in agriculture.IMPORTANCEBacillus spp. are widely used as bioinoculants for plant growth promotion and disease suppression. The exertion of their plant-beneficial functions is largely dependent on their root colonization, which is closely related to their biofilm formation capabilities. On the other hand, Bacillus is the model bacterium for biofilm study, and the process and molecular network of biofilm formation are well characterized (B. Mielich-Süss and D. Lopez, Environ Microbiol 17:555-565, 2015, https://doi.org/10.1111/1462-2920.12527; L. S. Cairns, L. Hobley, and N. R. Stanley-Wall, Mol Microbiol 93:587-598, 2014, https://doi.org/10.1111/mmi.12697; H. Vlamakis, C. Aguilar, R. Losick, and R. Kolter, Genes Dev 22:945-953, 2008, https://doi.org/10.1101/gad.1645008; S. S. Branda, A. Vik, L. Friedman, and R. Kolter, Trends Microbiol 13:20-26, 2005, https://doi.org/10.1016/j.tim.2004.11.006; C. Aguilar, H. Vlamakis, R. Losick, and R. Kolter, Curr Opin Microbiol 10:638-643, 2007, https://doi.org/10.1016/j.mib.2007.09.006; S. S. Branda, J. E. González-Pastor, S. Ben-Yehuda, R. Losick, and R. Kolter, Proc Natl Acad Sci U S A 98:11621-11626, 2001, https://doi.org/10.1073/pnas.191384198). However, the identification and sensing of environmental signals triggering Bacillus biofilm formation need further research. Here, we report that the oxygen deficiency signal inducing Bacillus biofilm formation is sensed by the ResDE two-component regulatory system. Our results not only revealed the novel regulatory function of the ResDE two-component regulatory system but also identified the sensing system of a biofilm-triggering signal. This knowledge can help to enhance the biofilm formation and root colonization of plant-beneficial Bacillus strains and also provide new insights of bacterial biofilm formation regulation.

Dataset Information

Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans.

Publications

Novel two-component regulatory system involved in biofilm formation and acid resistance in Streptococcus mutans.

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