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Role of Tellurite Resistance Operon in Filamentous Growth of Yersinia pestis in Macrophages.

Ponnusamy D, Clinkenbeard KD - PLoS ONE (2015)

Bottom Line: Others have observed a filamentous response associated with expression of tellurite resistance operon in Escherichia coli exposed to tellurite.Further in E. coli, expression of Y. pestis terZAB, but not terCDE, conferred a filamentous phenotype.These findings support the role of Y. pestis terZAB mediation of the filamentous response phenotype; whereas, terCDE confers tellurite resistance.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078, United States of America.

ABSTRACT

Background: Yersinia pestis initiates infection by parasitism of host macrophages. In response to macrophage infections, intracellular Y. pestis can assume a filamentous cellular morphology which may mediate resistance to host cell innate immune responses. We previously observed the expression of Y. pestis tellurite resistance proteins TerD and TerE from the terZABCDE operon during macrophage infections. Others have observed a filamentous response associated with expression of tellurite resistance operon in Escherichia coli exposed to tellurite. Therefore, in this study we examine the potential role of Y. pestis tellurite resistance operon in filamentous cellular morphology during macrophage infections.

Principal findings: In vitro treatment of Y. pestis culture with sodium tellurite (Na2TeO3) caused the bacterial cells to assume a filamentous phenotype similar to the filamentous phenotype observed during macrophage infections. A deletion mutant for genes terZAB abolished the filamentous morphologic response to tellurite exposure or intracellular parasitism, but without affecting tellurite resistance. However, a terZABCDE deletion mutant abolished both filamentous morphologic response and tellurite resistance. Complementation of the terZABCDE deletion mutant with terCDE, but not terZAB, partially restored tellurite resistance. When the terZABCDE deletion mutant was complemented with terZAB or terCDE, Y. pestis exhibited filamentous morphology during macrophage infections as well as while these complemented genes were being expressed under an in vitro condition. Further in E. coli, expression of Y. pestis terZAB, but not terCDE, conferred a filamentous phenotype.

Conclusions: These findings support the role of Y. pestis terZAB mediation of the filamentous response phenotype; whereas, terCDE confers tellurite resistance. Although the beneficial role of filamentous morphological responses by Y. pestis during macrophage infections is yet to be fully defined, it may be a bacterial adaptive strategy to macrophage associated stresses.

No MeSH data available.


Related in: MedlinePlus

Minimal inhibitory concentrations and reductive phenotypesofY. pestis KIM6+ and ΔterZAB and ΔterZABCDE mutants for Na2TeO3exposure.(A) Y. pestis KIM6+ and ΔterZAB and ΔterZABCDE mutants were exposed to 2-fold serial dilutions of Na2TeO3overnight at 28°C, and the MIC determined as the lowest tellurite concentration with no growth observed. Asterisk represents significant difference between the mean values (** denotes p<0.01). LB agar plates containing 0.1mg/mL of Na2TeO3(C) or equivalent volume of PBS (B) inoculated with Y. pestis KIM6+ (1) and ΔterZAB (2) and ΔterZABCDE (3) mutants were incubated at 28°C for 2 to 3 days. Black colony color was associated with tellurite reductive phenotype.
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pone.0141984.g002: Minimal inhibitory concentrations and reductive phenotypesofY. pestis KIM6+ and ΔterZAB and ΔterZABCDE mutants for Na2TeO3exposure.(A) Y. pestis KIM6+ and ΔterZAB and ΔterZABCDE mutants were exposed to 2-fold serial dilutions of Na2TeO3overnight at 28°C, and the MIC determined as the lowest tellurite concentration with no growth observed. Asterisk represents significant difference between the mean values (** denotes p<0.01). LB agar plates containing 0.1mg/mL of Na2TeO3(C) or equivalent volume of PBS (B) inoculated with Y. pestis KIM6+ (1) and ΔterZAB (2) and ΔterZABCDE (3) mutants were incubated at 28°C for 2 to 3 days. Black colony color was associated with tellurite reductive phenotype.

Mentions: Y. pestis KIM6+ exhibited high level tellurite resistance with an MIC of 0.31 mg/mL (Fig 2A) and a black colony phenotype typical for the ter operon mediated tellurite reduction when plated on LB agar containing sub-inhibitory concentrations of Na2TeO3 (Fig 2C). The KIM6+ also exhibited a filamentous cellular morphology when grown in media containing sub-inhibitory concentrations of Na2TeO3 and intracellularly in RAW264.7 cells (Fig 3A and 3G).


Role of Tellurite Resistance Operon in Filamentous Growth of Yersinia pestis in Macrophages.

Ponnusamy D, Clinkenbeard KD - PLoS ONE (2015)

Minimal inhibitory concentrations and reductive phenotypesofY. pestis KIM6+ and ΔterZAB and ΔterZABCDE mutants for Na2TeO3exposure.(A) Y. pestis KIM6+ and ΔterZAB and ΔterZABCDE mutants were exposed to 2-fold serial dilutions of Na2TeO3overnight at 28°C, and the MIC determined as the lowest tellurite concentration with no growth observed. Asterisk represents significant difference between the mean values (** denotes p<0.01). LB agar plates containing 0.1mg/mL of Na2TeO3(C) or equivalent volume of PBS (B) inoculated with Y. pestis KIM6+ (1) and ΔterZAB (2) and ΔterZABCDE (3) mutants were incubated at 28°C for 2 to 3 days. Black colony color was associated with tellurite reductive phenotype.
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Related In: Results  -  Collection

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pone.0141984.g002: Minimal inhibitory concentrations and reductive phenotypesofY. pestis KIM6+ and ΔterZAB and ΔterZABCDE mutants for Na2TeO3exposure.(A) Y. pestis KIM6+ and ΔterZAB and ΔterZABCDE mutants were exposed to 2-fold serial dilutions of Na2TeO3overnight at 28°C, and the MIC determined as the lowest tellurite concentration with no growth observed. Asterisk represents significant difference between the mean values (** denotes p<0.01). LB agar plates containing 0.1mg/mL of Na2TeO3(C) or equivalent volume of PBS (B) inoculated with Y. pestis KIM6+ (1) and ΔterZAB (2) and ΔterZABCDE (3) mutants were incubated at 28°C for 2 to 3 days. Black colony color was associated with tellurite reductive phenotype.
Mentions: Y. pestis KIM6+ exhibited high level tellurite resistance with an MIC of 0.31 mg/mL (Fig 2A) and a black colony phenotype typical for the ter operon mediated tellurite reduction when plated on LB agar containing sub-inhibitory concentrations of Na2TeO3 (Fig 2C). The KIM6+ also exhibited a filamentous cellular morphology when grown in media containing sub-inhibitory concentrations of Na2TeO3 and intracellularly in RAW264.7 cells (Fig 3A and 3G).

Bottom Line: Others have observed a filamentous response associated with expression of tellurite resistance operon in Escherichia coli exposed to tellurite.Further in E. coli, expression of Y. pestis terZAB, but not terCDE, conferred a filamentous phenotype.These findings support the role of Y. pestis terZAB mediation of the filamentous response phenotype; whereas, terCDE confers tellurite resistance.

View Article: PubMed Central - PubMed

Affiliation: Department of Veterinary Pathobiology, Center for Veterinary Health Sciences, Oklahoma State University, Stillwater, OK 74078, United States of America.

ABSTRACT

Background: Yersinia pestis initiates infection by parasitism of host macrophages. In response to macrophage infections, intracellular Y. pestis can assume a filamentous cellular morphology which may mediate resistance to host cell innate immune responses. We previously observed the expression of Y. pestis tellurite resistance proteins TerD and TerE from the terZABCDE operon during macrophage infections. Others have observed a filamentous response associated with expression of tellurite resistance operon in Escherichia coli exposed to tellurite. Therefore, in this study we examine the potential role of Y. pestis tellurite resistance operon in filamentous cellular morphology during macrophage infections.

Principal findings: In vitro treatment of Y. pestis culture with sodium tellurite (Na2TeO3) caused the bacterial cells to assume a filamentous phenotype similar to the filamentous phenotype observed during macrophage infections. A deletion mutant for genes terZAB abolished the filamentous morphologic response to tellurite exposure or intracellular parasitism, but without affecting tellurite resistance. However, a terZABCDE deletion mutant abolished both filamentous morphologic response and tellurite resistance. Complementation of the terZABCDE deletion mutant with terCDE, but not terZAB, partially restored tellurite resistance. When the terZABCDE deletion mutant was complemented with terZAB or terCDE, Y. pestis exhibited filamentous morphology during macrophage infections as well as while these complemented genes were being expressed under an in vitro condition. Further in E. coli, expression of Y. pestis terZAB, but not terCDE, conferred a filamentous phenotype.

Conclusions: These findings support the role of Y. pestis terZAB mediation of the filamentous response phenotype; whereas, terCDE confers tellurite resistance. Although the beneficial role of filamentous morphological responses by Y. pestis during macrophage infections is yet to be fully defined, it may be a bacterial adaptive strategy to macrophage associated stresses.

No MeSH data available.


Related in: MedlinePlus