The Staphylococcus aureus KdpDE Two-Component System Couples Extracellular K
            <sup>+</sup>
            Sensing and Agr Signaling to Infection Programming

Xue, Ting; You, Yibo; De, Hong; Sun, Haipeng; Sun, Bo

doi:10.1128/iai.01180-10

Cited by 88 publications

(104 citation statements)

References 55 publications

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“…This ATP-dependent potassium uptake system has been best characterized in E. coli and consists of four membrane components KdpABCF and the twocomponent system KdpDE, which is required for KdpABCF expression at a very low potassium concentration when the other uptake systems are no longer sufficient to allow the cell to acquire the necessary amount of ion (31). However, a recent study on the S. aureus KdpDE system suggested that this two-component system has a different function in this organism (32). The S. aureus KdpDE two-component system, which still responds to the extracellular potassium concentration, was found to be no longer required for bacterial survival under low potassium conditions, but instead to control the expression of several well-characterized S. aureus virulence factors (32).…”

Section: Discussionmentioning

confidence: 99%

“…However, a recent study on the S. aureus KdpDE system suggested that this two-component system has a different function in this organism (32). The S. aureus KdpDE two-component system, which still responds to the extracellular potassium concentration, was found to be no longer required for bacterial survival under low potassium conditions, but instead to control the expression of several well-characterized S. aureus virulence factors (32). However, additional work is needed to fully understand the function of this two-component system in S. aureus and other Gram-positive bacteria and on the basis of this study its interplay with cellular c-di-AMP levels.…”

Section: Discussionmentioning

confidence: 99%

“…Protein concentrations were determined by A 280 readings. 32 P-labeled c-di-AMP was dispensed into 96-well plates containing E. coli lysates, and aliquots were subsequently spotted in duplicate onto nitrocellulose membrane. The fraction of bound c-di-AMP was calculated for each well as described by Roelofs et al (27) and the average values from the duplicate spots plotted.…”

Section: Methodsmentioning

confidence: 99%

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Systematic identification of conserved bacterial c-di-AMP receptor proteins

Corrigan

Campeotto

Jeganathan

et al. 2013

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

266

405

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Nucleotide signaling molecules are important messengers in key pathways that allow cellular responses to changing environments. Canonical secondary signaling molecules act through specific receptor proteins by direct binding to alter their activity. Cyclic diadenosine monophosphate (c-di-AMP) is an essential signaling molecule in bacteria that has only recently been discovered. Here we report on the identification of four Staphylococcus aureus c-di-AMP receptor proteins that are also widely distributed among other bacteria. Using an affinity pull-down assay we identified the potassium transporter-gating component KtrA as a c-di-AMP receptor protein, and it was further shown that this protein, together with c-di-AMP, enables S. aureus to grow in low potassium conditions. We defined the c-di-AMP binding activity within KtrA to the RCK_C ( r egulator of c onductance of K + ) domain. This domain is also found in a second S. aureus protein, a predicted cation/proton antiporter, CpaA, which as we show here also directly binds c-di-AMP. Because RCK_C domains are found in proteinaceous channels, transporters, and antiporters from all kingdoms of life, these findings have broad implications for the regulation of different pathways through nucleotide-dependent signaling. Using a genome-wide nucleotide protein interaction screen we further identified the histidine kinase protein KdpD that in many bacteria is also involved in the regulation of potassium transport and a P II-like s ignal t ransduction protein, which we renamed PstA, as c-di-AMP binding proteins. With the identification of these widely distributed c-di-AMP receptor proteins we link the c-di-AMP signaling network to a central metabolic process in bacteria.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

Systematic identification of conserved bacterial c-di-AMP receptor proteins

Corrigan

Campeotto

Jeganathan

et al. 2013

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

266

405

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“…In some bacteria, extracellular K ϩ can act as a signal cation to activate virulence mechanisms (50)(51)(52). In S. mutans Ingbritt, the addition of K ϩ increased the rate of acid production, which is an essential virulence factor (14).…”

Section: Discussionmentioning

confidence: 99%

Trk2 Potassium Transport System in Streptococcus mutans and Its Role in Potassium Homeostasis, Biofilm Formation, and Stress Tolerance

et al. 2016

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Potassium (K؉ ) is the most abundant cation in the fluids of dental biofilm. The biochemical and biophysical functions of K ؉ and a variety of K ؉ transport systems have been studied for most pathogenic bacteria but not for oral pathogens. In this study, we establish the modes of K ؉ acquisition in Streptococcus mutans and the importance of K ؉ homeostasis for its virulence attributes. The S. mutans genome harbors four putative K ؉ transport systems that included two Trk-like transporters (designated Trk1 and Trk2), one glutamate/K ؉ cotransporter (GlnQHMP), and a channel-like K ؉ transport system (Kch). Mutants lacking Trk2 had significantly impaired growth, acidogenicity, aciduricity, and biofilm formation. [K ؉ ] less than 5 mM eliminated biofilm formation in S. mutans. The functionality of the Trk2 system was confirmed by complementing an Escherichia coli TK2420 mutant strain, which resulted in significant K ؉ accumulation, improved growth, and survival under stress. Taken together, these results suggest that Trk2 is the main facet of the K ؉ -dependent cellular response of S. mutans to environment stresses. IMPORTANCEBiofilm formation and stress tolerance are important virulence properties of caries-causing Streptococcus mutans. To limit these properties of this bacterium, it is imperative to understand its survival mechanisms. Potassium is the most abundant cation in dental plaque, the natural environment of S. mutans. K ؉ is known to function in stress tolerance, and bacteria have specialized mechanisms for its uptake. However, there are no reports to identify or characterize specific K ؉ transporters in S. mutans. We identified the most important system for K ؉ homeostasis and its role in the biofilm formation, stress tolerance, and growth. We also show the requirement of environmental K ؉ for the activity of biofilm-forming enzymes, which explains why such high levels of K ؉ would favor biofilm formation. Bacteria utilize specialized endogenous mechanisms to survive and proliferate in transient environments. A common bacterial response to environmental perturbations, such as acid stress, osmotic tension, and nutrient deprivation, is to accumulate certain solutes, such as potassium (K ϩ ). K ϩ , a naturally abundant cation, is present in all types of cells and is essential for both cell survival and physiology. K ϩ accumulation under stress conditions enables organisms to contend with dehydration, membrane damage, regulation of the Na ϩ /H ϩ -dependent cell energetics, and pH homeostasis while simultaneously minimizing interference with the structures and functions of intracellular proteins (1-3).In prokaryotes, four main K ϩ transport systems have been identified, which include the proteins Trk (or Ktr), Kdp, Kup, and channel-like Kch (4), all of which have different K ϩ affinities. Their variety and independent functioning have likely evolved as a cell survival strategy to ensure that adequate levels of K ϩ are present at all times to contend with environmental changes (5). These systems are r...

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“…We identified the SCCmec type V element, which is different from that of ST772. Two virulence determinants, a kdp operon (virulence regulator during pathogenesis) and an arginine deiminase locus comprising arcC, arcD, arcB, arcA, and argR genes, not detected by microarray, were found in the genome sequence and later validated by PCR (8).…”

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confidence: 99%

Draft Genome Sequence of Staphylococcus aureus ST672, an Emerging Disease Clone from India

Khedkar

Prabhakara²,

Loganathan³

et al. 2012

J Bacteriol

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We report the draft genome sequence of methicillin-resistant Staphylococcus aureus (MRSA) strain ST672, an emerging disease clone in India, from a septicemia patient. The genome size is about 2.82 Mb with 2,485 open reading frames (ORFs). The staphylococcal cassette chromosome mec (SCCmec) element (type V) and immune evasion cluster appear to be different from those of strain ST772 on preliminary examination. Methicillin-resistant Staphylococcus aureus (MRSA) epidemiology has undergone tremendous changes since the advent of community-associated MRSA containing staphylococcal cassette chromosome mec (SCCmec) elements type IV and V in the 1990s (1, 2). Although these strains originated in the community, they have successfully invaded hospitals and are replacing traditionally hospital-associated MRSA with SCCmec element types I, II, and III (5).The major clones of MRSA present in Indian hospitals and the community are ST22 EMRSA-15 (SCCmec type IV) and ST772 (SCCmec type V). In addition, there is a new and emerging clone, ST672, which we have characterized as carrying SCCmec type V, agr type I, and capsular polysaccharide type 8 and as PantonValentine leukocidin (PVL) negative by microarray (7). The allelic pattern for ST672 derived from the multilocus sequence type (MLST) database is 4-3-1-1-11-72-11 for the seven housekeeping genes. Coombs et al. from Australia have reported ST672 carrying SCCmec element IVa as well as V (3). Our collection includes three carrier methicillin-susceptible S. aureus (MSSA) isolates from nasal swabs of outpatients in a hospital, two disease MRSA isolates from blood and pus, and one MSSA isolate from an eye infection. The spa types of carrier isolates are t3840 and t3841, and all disease isolates have spa type t1309. Here we report the draft genome sequence of an S. aureus ST672 strain named GR1 (spa type t1309), isolated from the blood of a septicemia patient.Genomic DNA from GR1 (ST672) was fragmented to 300 to 400 bp, and paired-end sequencing was performed on an Illumina HiSeq-1000 sequencer. About 11 million paired-end reads (75 nucleotides [nt] each) were obtained, of which ϳ9.8 million reads (ϳ250-fold coverage) passed a quality filter with the following criteria: average read quality score of at least 35, minimum base quality of 30, and no undetermined base. We randomly sampled 20% of the reads to obtain a 50-fold coverage of the genome. Three such random read samples were obtained and assembled using Velvet (9).The reads were assembled into 64, 73, and 71 contigs, respectively, for the three assemblies, covering ϳ2.82 million base pairs. For quality assessment, we mapped all the raw reads back to the contigs. This analysis gave insert size distribution in the expected range and comparable to USA300 sequence reads (6). When aligned against fully sequenced S. aureus genomes using BLASTN (E value, Ͻ10 Ϫ100 ), we found ϳ89 to 94% similarity.GLIMMER predicted 2,485 open reading frames (ORFs) in at least two of three assemblies, of which 2,298 (92%) showed homology to ORFs in other...

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The Staphylococcus aureus KdpDE Two-Component System Couples Extracellular K ⁺ Sensing and Agr Signaling to Infection Programming

Cited by 88 publications

References 55 publications

Systematic identification of conserved bacterial c-di-AMP receptor proteins

Systematic identification of conserved bacterial c-di-AMP receptor proteins

Trk2 Potassium Transport System in Streptococcus mutans and Its Role in Potassium Homeostasis, Biofilm Formation, and Stress Tolerance

Draft Genome Sequence of Staphylococcus aureus ST672, an Emerging Disease Clone from India

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The Staphylococcus aureus KdpDE Two-Component System Couples Extracellular K + Sensing and Agr Signaling to Infection Programming

Cited by 88 publications

References 55 publications

Systematic identification of conserved bacterial c-di-AMP receptor proteins

Systematic identification of conserved bacterial c-di-AMP receptor proteins

Trk2 Potassium Transport System in Streptococcus mutans and Its Role in Potassium Homeostasis, Biofilm Formation, and Stress Tolerance

Draft Genome Sequence of Staphylococcus aureus ST672, an Emerging Disease Clone from India

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The Staphylococcus aureus KdpDE Two-Component System Couples Extracellular K ⁺ Sensing and Agr Signaling to Infection Programming