Co‐ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species

Kreth, Jens; Merritt, Justin; Shi, Wenyuan; Qi, Fengxia

doi:10.1111/j.1365-2958.2005.04695.x

Cited by 181 publications

(220 citation statements)

References 53 publications

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“…In P. aeruginosa, eDNA release depends on quorum sensing (35), and there is evidence to suggest that cell lysis itself may be achieved by prophage induction within a biofilm (38,50), or alternatively, as a consequence of the release of membrane vesicles that contain bacteriolytic activity (51,52) as well as DNA (53). In Streptococcus mutans and Streptococcus pneumoniae, DNA is released from a lysing subfraction of the bacterial population in response to competence development, a physiological process that also depends on quorum sensing (54)(55)(56)(57)(58)(59). Both the actions of bacteriocins (59-61) and autolysins (56,58) have been implicated in the lysis of DNA-releasing cells during this process.…”

Section: Discussionmentioning

confidence: 99%

The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus

Rice

Mann

Endres

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

589

658

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The Staphylococcus aureus cidA and lrgA genes have been shown to affect cell lysis under a variety of conditions during planktonic growth. It is hypothesized that these genes encode holins and antiholins, respectively, and may serve as molecular control elements of bacterial cell lysis. To examine the biological role of cell death and lysis, we studied the impact of the cidA mutation on biofilm development. Interestingly, this mutation had a dramatic impact on biofilm morphology and adherence. The cidA mutant (KB1050) biofilm exhibited a rougher appearance compared with the parental strain (UAMS-1) and was less adherent. Propidium iodide staining revealed that KB1050 accumulated more dead cells within the biofilm population relative to UAMS-1, indicative of reduced cell lysis. In agreement with this finding, quantitative real-time PCR experiments demonstrated the presence of 5-fold less genomic DNA in the KB1050 biofilm relative to UAMS-1. Furthermore, treatment of the UAMS-1 biofilm with DNase I caused extensive cell detachment, whereas similar treatment of the KB1050 biofilm had only a modest effect. These results demonstrate that cidA-controlled cell lysis plays a significant role during biofilm development and that released genomic DNA is an important structural component of S. aureus biofilm.autolysis ͉ extracellular DNA ͉ programmed cell death ͉ holin

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Section: Discussionmentioning

confidence: 99%

The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus

Rice

Mann

Endres

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

589

658

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“…As we later found in this study, the S. mutans GS5 wild-type strain had a prominent "sticky phenotype" that was not apparent with the UA159 strain. Therefore, chromosomal DNA isolated from SmuvicX with a DNeasy tissue kit (QIAGEN, Valencia, CA) was used to transform S. mutans GS5 in the presence of synthetic competence-stimulating peptide (CSP), whose sequence corresponds to the sequence of the natural GS5 autoinducer peptide (16). VicXdeficient erythromycin-resistant (10 g/ml) transformants were isolated, and the allelic exchange event was confirmed by PCR using the same combination of primers that was used to confirm the vicX null mutation in the SmuvicX mutant strain.…”

Section: Methodsmentioning

confidence: 99%

The Streptococcus mutans vicX Gene Product Modulates gtfB / C Expression, Biofilm Formation, Genetic Competence, and Oxidative Stress Tolerance

et al. 2007

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Streptococcus mutans is considered one of the primary etiologic agents of dental caries. Previously, we characterized the VicRK two-component signal transduction system, which regulates multiple virulence factors of S. mutans. In this study, we focused on the vicX gene of the vicRKX tricistronic operon. To characterize vicX, we constructed a nonpolar deletion mutation in the vicX coding region in S. mutans UA159. The growth kinetics of the mutant (designated SmuvicX) showed that the doubling time was longer and that there was considerable sensitivity to paraquat-induced oxidative stress. Supplementing a culture of the wild-type UA159 strain with paraquat significantly increased the expression of vicX (P < 0.05, as determined by analysis of variance [ANOVA]), confirming the role of this gene in oxidative stress tolerance in S. mutans. Examination of mutant biofilms revealed architecturally altered cell clusters that were seemingly denser than the wild-type cell clusters. Interestingly, vicX-deficient cells grown in a glucose-supplemented medium exhibited significantly increased glucosyltransferase B/C (gtfB/C) expression compared with the expression in the wild type (P < 0.05, as determined by ANOVA). Moreover, a sucrose-dependent adhesion assay performed using an S. mutans GS5-derived vicX null mutant demonstrated that the adhesiveness of this mutant was enhanced compared with that of the parent strain and isogenic mutants of the parent strain lacking gtfB and/or gtfC. Also, disruption of vicX reduced the genetic transformability of the mutant approximately 10-fold compared with that of the parent strain (P < 0.05, as determined by ANOVA). Collectively, these findings provide insight into important phenotypes controlled by the vicX gene product that can impact S. mutans pathogenicity.

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“…Interestingly, we have previously observed that the expression of at least two bacteriocins (mutacins) of S. mutans is largely dependent upon a cell density similar to that attained in the dental plaque or within a cell colony. While both bacteriocins normally exhibit little or no expression in broth cultures, we have demonstrated that the centrifugation and incubation of pelleted exponential-phase cultures can strongly induce the expression of both bacteriocins (Kreth et al, 2005;Merritt et al, 2005b). Thus we hypothesized that bacteriocin expression may be controlled by densitydependent regulators that are responsive to extremely high cell density.…”

Section: Introductionmentioning

confidence: 99%

Genetic characterization of the hdrRM operon: a novel high-cell-density-responsive regulator in Streptococcus mutans

et al. 2007

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Many species of bacteria can adhere to surfaces and grow as sessile communities. The continued accumulation of bacteria can eventually lead to the extremely high-cell-density environment characteristic of many biofilms or cell colonies. This is the normal habitat of the cariogenic species Streptococcus mutans, which normally resides in the high-cell-density, multispecies community commonly referred to as dental plaque. Previous work has demonstrated that the transcription of two separate bacteriocins can be activated by the high-cell-density conditions created through the centrifugation and incubation of cell pellets. In this study, we identified an uncharacterized two-gene operon that was induced .10-fold by conditions of high cell density. The genes of the operon encode a putative transcription regulator and a membrane protein, which were renamed as hdrR and hdrM, respectively. A transcription fusion to the hdrRM operon confirmed its induction by high cell density. Mutation of hdrM abolished bacteriocin production, greatly increased natural competence, reduced the growth rate, and severely affected biofilm formation. Interestingly, no obvious phenotypes were observed from a non-polar mutation of hdrR or mutations affecting the entire operon. These data suggest that the hdrRM operon may constitute a novel regulatory system responsible for mediating a cellular response to a high-cell-density environment.

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Co‐ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species

Cited by 181 publications

References 53 publications

The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus

The cidA murein hydrolase regulator contributes to DNA release and biofilm development in Staphylococcus aureus

The Streptococcus mutans vicX Gene Product Modulates gtfB / C Expression, Biofilm Formation, Genetic Competence, and Oxidative Stress Tolerance

Genetic characterization of the hdrRM operon: a novel high-cell-density-responsive regulator in Streptococcus mutans

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