Staphylococcal NreB: an O<sub>2</sub>‐sensing histidine protein kinase with an O<sub>2</sub>‐labile iron–sulphur cluster of the FNR type

Kamps, A. M. I. E.; Achebach, Stephanie; Fedtke, Iris; Unden, Gottfried; Götz, Friedrich

doi:10.1111/j.1365-2958.2004.04024.x

Cited by 59 publications

(67 citation statements)

References 43 publications

(79 reference statements)

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“…As stated previously, S. aureus can use oxygen, nitrate, or nitrite as electron acceptors in the electron transfer chain; thus, S. aureus must have a means to "sense" the presence or absence of these electron acceptors. S. aureus uses a two-component regulatory system encoded by NreABC that consists of a histidine sensor kinase (NreB) and a response regulator (NreC) (112,192); the function of NreA has yet to be determined. NreB is a cytoplasmic protein that contains a cysteine-coordinated, oxygen-sensitive, iron-sulfur cluster similar to the fumarate nitrate reductase regulator (112).…”

Section: Nitrogen-dependent Regulatorsmentioning

confidence: 99%

“…S. aureus uses a two-component regulatory system encoded by NreABC that consists of a histidine sensor kinase (NreB) and a response regulator (NreC) (112,192); the function of NreA has yet to be determined. NreB is a cytoplasmic protein that contains a cysteine-coordinated, oxygen-sensitive, iron-sulfur cluster similar to the fumarate nitrate reductase regulator (112). Aerobic conditions cause the reversible loss of the iron-sulfur and dramatically reduce the autophosphorylation of NreB.…”

Section: Nitrogen-dependent Regulatorsmentioning

confidence: 99%

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At the Crossroads of Bacterial Metabolism and Virulence Factor Synthesis in Staphylococci

Somerville

Proctor

2009

Microbiol Mol Biol Rev

325

348

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SUMMARY Bacteria live in environments that are subject to rapid changes in the availability of the nutrients that are necessary to provide energy and biosynthetic intermediates for the synthesis of macromolecules. Consequently, bacterial survival depends on the ability of bacteria to regulate the expression of genes coding for enzymes required for growth in the altered environment. In pathogenic bacteria, adaptation to an altered environment often includes activating the transcription of virulence genes; hence, many virulence genes are regulated by environmental and nutritional signals. Consistent with this observation, the regulation of most, if not all, virulence determinants in staphylococci is mediated by environmental and nutritional signals. Some of these external signals can be directly transduced into a regulatory response by two-component regulators such as SrrAB; however, other external signals require transduction into intracellular signals. Many of the external environmental and nutritional signals that regulate virulence determinant expression can also alter bacterial metabolic status (e.g., iron limitation). Altering the metabolic status results in the transduction of external signals into intracellular metabolic signals that can be “sensed” by regulatory proteins (e.g., CodY, Rex, and GlnR). This review uses information derived primarily using Bacillus subtilis and Escherichia coli to articulate how gram-positive pathogens, with emphasis on Staphylococcus aureus and Staphylococcus epidermidis, regulate virulence determinant expression in response to a changing environment.

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Section: Nitrogen-dependent Regulatorsmentioning

confidence: 99%

Section: Nitrogen-dependent Regulatorsmentioning

confidence: 99%

At the Crossroads of Bacterial Metabolism and Virulence Factor Synthesis in Staphylococci

Somerville

Proctor

2009

Microbiol Mol Biol Rev

325

348

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“…Another direct staphylococcal oxygen sensing system, NreABC (for nitrogen regulation), has been identified and characterized in S. carnosus (9). Upon oxygen depletion, autophosphorylation activity of the cytoplasmic histidine kinase NreB increases, which depends on the formation of an oxygen-labile iron-sulfur cluster (16). The response regulator NreC is phosphorylated by NreB and specifically binds to the promoters of the nitrate reductase and nitrite reductase operons and of the narT gene to enhance transcription (9).…”

mentioning

confidence: 99%

“…NreA almost exclusively consists of a GAF domain, which is one of the largest families of cyclic nucleotide-binding regulatory domains (18). In S. aureus, genes homologous to S. carnosus nreABC are present (16), and the respective proteins share 50%, 57%, and 85% identity (NreA [SA2181], NreB [SA2180], and NreC [SA2179], respectively).…”

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confidence: 99%

Characterization of the Oxygen-Responsive NreABC Regulon of Staphylococcus aureus

et al. 2008

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Here, we investigate the functionality of the oxygen-responsive nitrogen regulation system NreABC in the human pathogen Staphylococcus aureus and evaluate its role in anaerobic gene regulation and virulence factor expression. Deletion of nreABC resulted in severe impairment of dissimilatory nitrate and nitrite reduction and led to a small-colony phenotype in the presence of nitrate during anaerobic growth. For characterization of the NreABC regulon, comparative DNA microarray and proteomic analyses between the wild type and nreABC mutant were performed under anoxic conditions in the absence and presence of nitrate. A reduced expression of virulence factors was not observed in the mutant. However, both the transcription of genes involved in nitrate and nitrite reduction and the accumulation of corresponding proteins were highly decreased in the nreABC mutant, which was unable to utilize nitrate as a respiratory oxidant and, hence, was forced to use fermentative pathways. These data were corroborated by the quantification of the extracellular metabolites lactate and acetate. Using an Escherichia coli-compatible two-plasmid system, the activation of the promoters of the nitrate and nitrite reductase operons and of the putative nitrate/nitrite transporter gene narK by NreBC was confirmed. Overall, our data indicate that NreABC is very likely a specific regulation system that is essential for the transcriptional activation of genes involved in dissimilatory reduction and transport of nitrate and nitrite. The study underscores the importance of NreABC as a fitness factor for S. aureus in anoxic environments.

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“…In Escherichia coli, a global regulator, Fnr (fumarate and nitrate reductase regulation), controls gene expression in response to anaerobic environments by acting as a sensor and a regulator (31); however, in S. aureus no Fnr homolog seems to exist (30). The oxygen-liable iron-sulfur cluster of the NreBC system senses oxygen depletion and regulates anaerobic gene expression in S. aureus (12).…”

mentioning

confidence: 99%

The Essential Two-Component System YhcSR Is Involved in Regulation of the Nitrate Respiratory Pathway of Staphylococcus aureus

Yan

Yang

et al. 2011

Journal of Bacteriology

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Our previous studies revealed that a novel two-component signal transduction system, YhcSR, is essential for the survival of Staphylococcus aureus; however, the biological function of YhcSR remains unknown. In this study, we demonstrated that YhcSR plays an important role in the modulation of the nitrate respiratory pathway under anaerobic conditions. Specifically, we determined that nitrate induces yhcS transcription in the early log phase of growth under anaerobic conditions and that the downregulation of yhcSR expression eliminates the stimulatory effect of nitrate on bacterial growth. Using semiquantitative real-time reverse transcription-PCR (qPCR) and promoter-lux reporter fusions, we established that YhcSR positively modulates the transcription of the narG operon, which is involved in the nitrate respiratory pathway. Our gel shift assays revealed that YhcR binds to the promoter regions of narG and nreABC. Collectively, the above data indicate that the yhcSR system directly regulates the expression of both narG and nreABC operons, which in turn positively modulate the nitrate respiratory pathway of S. aureus under anaerobic conditions. These results provide a new insight into the biological functions of the essential two-component YhcSR system.

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Staphylococcal NreB: an O₂‐sensing histidine protein kinase with an O₂‐labile iron–sulphur cluster of the FNR type

Cited by 59 publications

References 43 publications

At the Crossroads of Bacterial Metabolism and Virulence Factor Synthesis in Staphylococci

At the Crossroads of Bacterial Metabolism and Virulence Factor Synthesis in Staphylococci

Characterization of the Oxygen-Responsive NreABC Regulon of Staphylococcus aureus

The Essential Two-Component System YhcSR Is Involved in Regulation of the Nitrate Respiratory Pathway of Staphylococcus aureus

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Staphylococcal NreB: an O2‐sensing histidine protein kinase with an O2‐labile iron–sulphur cluster of the FNR type

Cited by 59 publications

References 43 publications

At the Crossroads of Bacterial Metabolism and Virulence Factor Synthesis in Staphylococci

At the Crossroads of Bacterial Metabolism and Virulence Factor Synthesis in Staphylococci

Characterization of the Oxygen-Responsive NreABC Regulon of Staphylococcus aureus

The Essential Two-Component System YhcSR Is Involved in Regulation of the Nitrate Respiratory Pathway of Staphylococcus aureus

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Staphylococcal NreB: an O₂‐sensing histidine protein kinase with an O₂‐labile iron–sulphur cluster of the FNR type