Catabolite Control Protein A Controls Hydrogen Peroxide Production and Cell Death in<i>Streptococcus sanguinis</i>

Zheng, Lan; Chen, Zhijun; Itzek, Andreas; Ashby, Michael T.; Kreth, Jens

doi:10.1128/jb.01131-10

Cited by 70 publications

(99 citation statements)

References 46 publications

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“…Previously, it was reported that eDNA release of S. gordonii could be stimulated by 1 mM H 2 O 2 and occurred without detectable lysis of the cells (30). More recently, Zheng and coworkers showed that H 2 O 2 production by pyruvate oxidase is a contributing factor to lysis of S. sanguinis, a close relative of S. gordonii (74). In this study, we observed that 0.003% H 2 O 2 (4) was not sufficient to trigger cell lysis of S. gordonii (Fig.…”

Section: Discussionmentioning

confidence: 99%

The Major Autolysin of Streptococcus gordonii Is Subject to Complex Regulation and Modulates Stress Tolerance, Biofilm Formation, and Extracellular-DNA Release

Liu

Burne

2011

J Bacteriol

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A gene, designated atlS, encoding a major autolysin from Streptococcus gordonii, was identified and characterized. The predicted AtlS protein is 1,160 amino acids and 127 kDa and has a conserved ␤1,4-N-acetylmuramidase domain. Zymographic analysis of wild-type S. gordonii revealed peptidoglycan hydrolase activities with molecular masses of 130 and 90 kDa that were absent in an atlS deletion mutant. Western blotting revealed that the 90-kDa band was derived from the 130-kDa protein. Inactivation of atlS resulted in formation of long chains by the cells, markedly decreased autolytic capacity, poor biofilm formation, diminished tolerance of acid and oxidative stress, and decreased production of extracellular DNA (eDNA). The biofilm-forming capacity of the atlS mutant could be almost completely restored to that of the wild-type strain by adding purified recombinant AtlA autolysin of S. mutans but was only partially restored by addition of eDNA. Autolysis, eDNA release, and atlS expression increased sharply when cells entered stationary phase and were greatly enhanced in cells growing with aeration. The LytST and VicRK two-component systems were both required for the induction of atlS by aeration, and purified LytT was able to bind to the promoter region of atlS in vitro. Thus, AtlS and its associated regulatory cascade dominantly control phenotypes of S. gordonii that are critical to colonization, persistence, and competition with other commensal and pathogenic oral bacteria in response to the redox environment and growth domain.Autolysis, which is triggered by a self-digestion of the cell wall by peptidoglycan hydrolases, can be a mechanism for programmed cell death in bacteria but also plays critical roles in cell wall turnover, cell separation, antibiotic resistance, adherence, genetic competence, and protein secretion (10,23,25,41,61).

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Section: Discussionmentioning

confidence: 99%

The Major Autolysin of Streptococcus gordonii Is Subject to Complex Regulation and Modulates Stress Tolerance, Biofilm Formation, and Extracellular-DNA Release

Liu

Burne

2011

J Bacteriol

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“…In support of this, we demonstrate that the presence of NanA dramatically increased the exposure of non-CCR-acting galactose on the surface of septal epithelial cells in vivo. Moreover, that spxB gene, whose expression is suppressed by glucose-mediated CCR and derepressed under growth in galactose (26,27), was essential for biofilm formation in vitro and in vivo. The latter in vivo result was recently published by our group (29).…”

Section: Discussionmentioning

confidence: 99%

“…Pyruvate oxidase is a key enzyme in the non-lactic acid-producing metabolic pathway in S. pneumoniae, and its homologues are under catabolite repression in a number of bacterial species. Encoded by spxB, pyruvate oxidase-dependent metabolism results in the conversion of pyruvate to acetyl-phosphate, which is a precursor for fatty acid biosynthesis and amino acids such as leucine (26,27). During this process, hydrogen peroxide is generated, which has been shown to be a virulence determinant (28).…”

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confidence: 99%

Neuraminidase A-Exposed Galactose Promotes Streptococcus pneumoniae Biofilm Formation during Colonization

et al. 2016

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f Streptococcus pneumoniae is an opportunistic pathogen that colonizes the nasopharynx. Herein we show that carbon availability is distinct between the nasopharynx and bloodstream of adult humans: glucose is absent from the nasopharynx, whereas galactose is abundant. We demonstrate that pneumococcal neuraminidase A (NanA), which cleaves terminal sialic acid residues from host glycoproteins, exposed galactose on the surface of septal epithelial cells, thereby increasing its availability during colonization. We observed that S. pneumoniae mutants deficient in NanA and ␤-galactosidase A (BgaA) failed to form biofilms in vivo despite normal biofilm-forming abilities in vitro. Subsequently, we observed that glucose, sucrose, and fructose were inhibitory for biofilm formation, whereas galactose, lactose, and low concentrations of sialic acid were permissive. Together these findings suggested that the genes involved in biofilm formation were under some form of carbon catabolite repression (CCR), a regulatory network in which genes involved in the uptake and metabolism of less-preferred sugars are silenced during growth with preferred sugars. Supporting this notion, we observed that a mutant deficient in pyruvate oxidase, which converts pyruvate to acetyl-phosphate under non-CCR-inducing growth conditions, was unable to form biofilms. Subsequent comparative transcriptome sequencing (RNA-seq) analyses of planktonic and biofilm-grown pneumococci showed that metabolic pathways involving the conversion of pyruvate to acetyl-phosphate and subsequently leading to fatty acid biosynthesis were consistently upregulated during diverse biofilm growth conditions. We conclude that carbon availability in the nasopharynx impacts pneumococcal biofilm formation in vivo. Additionally, biofilm formation involves metabolic pathways not previously appreciated to play an important role.

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“…Real-time PCR (RT-PCR) was performed to detect specific transcripts with the comparative threshold cycle (C T ) method using a MyiQ single-color real-time PCR detection system (Bio-Rad). Relative changes in gene expression were calculated using the ⌬C T method described previously (62). The 16S rRNA gene was used as the housekeeping reference gene using the 16S rRNA primers described above.…”

Section: Methodsmentioning

confidence: 99%

Hydrogen Peroxide-Dependent DNA Release and Transfer of Antibiotic Resistance Genes in Streptococcus gordonii

et al. 2011

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Certain oral streptococci produce H 2 O 2 under aerobic growth conditions to inhibit competing species like Streptococcus mutans. Additionally, H 2 O 2 production causes the release of extracellular DNA (eDNA). eDNA can participate in several important functions: biofilm formation and cell-cell aggregation are supported by eDNA, while eDNA can serve as a nutrient and as an antimicrobial agent by chelating essential cations. eDNA contains DNA fragments of a size that has the potential to transfer genomic information. By using Streptococcus gordonii as a model organism for streptococcal H 2 O 2 production, H 2 O 2 -dependent eDNA release was further investigated. Under defined growth conditions, the eDNA release process was shown to be entirely dependent on H 2 O 2 . Chromosomal DNA damage seems to be the intrinsic signal for the release, although only actively growing cells were proficient eDNA donors. Interestingly, the process of eDNA production was found to be coupled with the induction of the S. gordonii natural competence system. Consequently, the production of H 2 O 2 triggered the transfer of antibiotic resistance genes. These results suggest that H 2 O 2 is potentially much more than a simple toxic metabolic by-product; rather, its production could serve as an important environmental signal that facilitates species evolution by transfer of genetic information and an increase in the mutation rate.

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Catabolite Control Protein A Controls Hydrogen Peroxide Production and Cell Death inStreptococcus sanguinis

Cited by 70 publications

References 46 publications

The Major Autolysin of Streptococcus gordonii Is Subject to Complex Regulation and Modulates Stress Tolerance, Biofilm Formation, and Extracellular-DNA Release

The Major Autolysin of Streptococcus gordonii Is Subject to Complex Regulation and Modulates Stress Tolerance, Biofilm Formation, and Extracellular-DNA Release

Neuraminidase A-Exposed Galactose Promotes Streptococcus pneumoniae Biofilm Formation during Colonization

Hydrogen Peroxide-Dependent DNA Release and Transfer of Antibiotic Resistance Genes in Streptococcus gordonii

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