Mg2+ Sensing by the Mg2+ Sensor PhoQ of Salmonella enterica

Chamnongpol, Sangpen; Cromie, Michael J.; Groisman, Eduardo A.

doi:10.1016/s0022-2836(02)01268-8

Cited by 82 publications

(84 citation statements)

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“…In addition, PmrD (encoded by the pmrD gene) can activate signaling through the PmrAB pathway in a posttranslational manner, and the expression of pmrD is under the control of the PhoPQ two-component pathway (33). PhoPQ responds to the level of Mg 2ϩ in the environment, and, therefore, the expression of the pmrHFIJKLM operon can also be regulated by the level of Mg 2ϩ in an Fe 3ϩ -independent manner (10,33). In silico analysis of the genome sequence of TT01 does reveal the presence of homologues of phoP and phoQ (plu2807 and plu2808, respectively), but there is no homologue of pmrA, pmrB, or pmrD.…”

Section: Discussionmentioning

confidence: 99%

ThepbgPEoperon inPhotorhabdus luminescensIs Required for Pathogenicity and Symbiosis

Bennett

Clarke

2005

J Bacteriol

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Photorhabdus is a genus of gram-negative Enterobacteriaceae that is pathogenic to insect larvae while also maintaining a mutualistic relationship with nematodes from the family Heterorhabditis, where the bacteria occupy the gut of the infective juvenile (IJ) stage of the nematode. In this study we describe the identification and characterization of a mutation in the pbgE1 gene of Photorhabdus luminescens TT01, predicted to be the fifth gene in the pbgPE operon. We show that this mutant, BMM305, is strongly attenuated in virulence against larvae of the greater wax moth, Galleria mellonella, and we report that BMM305 is more sensitive to the cationic antimicrobial peptide, polymyxin B, and growth in mildly acidic pH than the parental strain of P. luminescens. Moreover, we also show that the lipopolysaccharide (LPS) present on the surface of BMM305 does not appear to contain any O antigen. Complementation studies reveal that the increased sensitivity to polymyxin B and growth in mildly acidic pH can be rescued by the in trans expression of pbgE1, while the defects in O-antigen assembly and pathogenicity require the in trans expression of pbgE1 and the downstream genes pbgE2 and pbgE3. Finally, we show that BMM305 is defective in symbiosis as this mutant is unable to colonize the gut of the IJ stage of the nematode. Therefore, we conclude that the pbgPE operon is required for both pathogenicity and symbiosis in P. luminescens.Photorhabdus is a genus of gram-negative, bioluminescent insect pathogenic bacteria that also has a mutualistic relationship with entomophagous nematodes from the family Heterorhabditis (8). The bacteria colonize the gut of the infective juvenile (IJ) stage of the nematode, a free-living, infectious stage that lives in the soil and actively seeks out insect larvae. The IJ enters the larva and regurgitates the bacteria into the hemolymph, where the bacteria multiply and kill the insect within 24 to 48 h of infection. The bacteria also produce a wide range of extracellular hydrolytic enzymes that function to convert the internal organs and tissues of the insect into a nutrient soup that can support nematode growth and development. After two to three generations within the insect, the nematodes develop into IJs, the bacteria recolonize the intestinal tract, and the IJs emerge from the cadaver in search of a new host (for a recent review, see reference 19).It has been suggested that pathogenicity and symbiosis share common molecular mechanisms and that the outcome of a bacterium-host interaction is the result of a negotiation between the organisms involved in the interaction (28). The Photorhabdus-nematode-insect tripartite system provides a useful model system in which this question can be directly addressed. DNA sequencing has revealed that Photorhabdus contains many genes predicted to encode proteins with homology to virulence factors characterized in other bacterial pathogens (16,20). Recent work has identified the Tc toxin, a large protein complex that is orally active against insect larvae, a...

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Section: Discussionmentioning

confidence: 99%

ThepbgPEoperon inPhotorhabdus luminescensIs Required for Pathogenicity and Symbiosis

Bennett

Clarke

2005

J Bacteriol

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“…Therefore, PhoP-dependent regulation was not involved in the observed activation of hilA-lacZ by Fur. This is not surprising because activation of PhoP by its cognate histidine kinase, PhoQ, is dependent on a low [Mg 2ϩ ], and it is likely that Mg 2ϩ is plentiful in the LB media used here (9,58).…”

Section: Vol 193 2011mentioning

confidence: 92%

Fur Negatively Regulates hns and Is Required for the Expression of HilA and Virulence in Salmonella enterica Serovar Typhimurium

et al. 2011

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Iron is an essential element for the survival of living cells. However, excess iron is toxic, and its uptake is exquisitely regulated by the ferric uptake regulator, Fur. In Salmonella, the Salmonella pathogenicity island 1 (SPI-1) encodes a type three secretion system, which is required for invasion of host epithelial cells in the small intestine. A major activator of SPI-1 is HilA, which is encoded within SPI-1. One known regulator of hilA is Fur. The mechanism of hilA regulation by Fur is unknown. We report here that Fur is required for virulence in Salmonella enterica serovar Typhimurium and that Fur is required for the activation of hilA, as well as of other HilA-dependent genes, invF and sipC. The Fur-dependent regulation of hilA was independent of PhoP, a known repressor of hilA. Instead, the expression of the gene coding for the histone-like protein, hns, was significantly derepressed in the fur mutant. Indeed, the activation of hilA by Fur was dependent on 28 nucleotides located upstream of hns. Moreover, we used chromatin immunoprecipitation to show that Fur bound, in vivo, to the upstream region of hns in a metal-dependent fashion. Finally, deletion of fur in an hns mutant resulted in Fur-independent activation of hilA. In conclusion, Fur activates hilA by repressing the expression of hns.

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“…1). In S. enterica, Chamnongpol et al 10) have evaluated how a D150, D151 and D152 acidic cluster of the PhoQ periplasmic region could be involved in regulating the target genes by extracellular Mg 2þ . They concluded in their study that the three residues within the acidic cluster (D150, 151 and 152) did not appear to be as critical as the conserved G93, W97, H120 and T156.…”

Section: Mutant Scanning Of Mg 2þ Sensor Phoq On Mgrb Expressionmentioning

confidence: 99%

“…7) However, in S. enterica, the residues within the acidic cluster contribute to a normal response to Mg 2þ , although they do not appear to be as critical as conserved residues G93, W97, H120 and T156 which are required for a wild-type response to Mg 2þ . 10) The known periplasmic mutants of PhoQ still responded to Mg 2þ to some extent, and no mutation was found to become fully constitutive. 5,6,10) We describe in this study the isolation and phenotypic characterization of 10 mutants with single-amino-acid substitutions in the periplasmic region (PhoQT47, T48, N68, D90, D149, D150, D151, D152 and D179) in Escherichia coli, finding that PhoQD179L(A) does not respond at all to either Mg 2þ or Ca 2þ .…”

mentioning

confidence: 98%

Isolation and Molecular Characterization of the Locked-on Mutant of Mg²⁺Sensor PhoQ inEscherichia coli

Minagawa

Okura

Tsuchitani

et al. 2005

Bioscience, Biotechnology, and Biochemistry

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Mg2+ Sensing by the Mg2+ Sensor PhoQ of Salmonella enterica

Cited by 82 publications

References 29 publications

ThepbgPEoperon inPhotorhabdus luminescensIs Required for Pathogenicity and Symbiosis

ThepbgPEoperon inPhotorhabdus luminescensIs Required for Pathogenicity and Symbiosis

Fur Negatively Regulates hns and Is Required for the Expression of HilA and Virulence in Salmonella enterica Serovar Typhimurium

Isolation and Molecular Characterization of the Locked-on Mutant of Mg²⁺Sensor PhoQ inEscherichia coli

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Mg2+ Sensing by the Mg2+ Sensor PhoQ of Salmonella enterica

Cited by 82 publications

References 29 publications

ThepbgPEoperon inPhotorhabdus luminescensIs Required for Pathogenicity and Symbiosis

ThepbgPEoperon inPhotorhabdus luminescensIs Required for Pathogenicity and Symbiosis

Fur Negatively Regulates hns and Is Required for the Expression of HilA and Virulence in Salmonella enterica Serovar Typhimurium

Isolation and Molecular Characterization of the Locked-on Mutant of Mg2+Sensor PhoQ inEscherichia coli

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Isolation and Molecular Characterization of the Locked-on Mutant of Mg²⁺Sensor PhoQ inEscherichia coli