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Mechanisms of pressure-mediated cell death and injury in Escherichia coli: from fundamentals to food applications.

Gänzle M, Liu Y - Front Microbiol (2015)

Bottom Line: High hydrostatic pressure is commercially applied to extend the shelf life of foods, and to improve food safety.The targeted design of processes for the safe elimination of E. coli thus necessitates deeper insights into mechanisms of interaction and matrix-strain interactions.The pressure-induced denaturation of membrane bound enzymes results in generation of reactive oxygen species and subsequent cell death caused by oxidative stress.

View Article: PubMed Central - PubMed

Affiliation: Department of Agricultural, Food and Nutritional Science, University of Alberta , Edmonton, AB, Canada.

ABSTRACT
High hydrostatic pressure is commercially applied to extend the shelf life of foods, and to improve food safety. Current applications operate at ambient temperature and 600 MPa or less. However, bacteria that may resist this pressure level include the pathogens Staphylococcus aureus and strains of Escherichia coli, including shiga-toxin producing E. coli. The resistance of E. coli to pressure is variable between strains and highly dependent on the food matrix. The targeted design of processes for the safe elimination of E. coli thus necessitates deeper insights into mechanisms of interaction and matrix-strain interactions. Cellular targets of high pressure treatment in E. coli include the barrier properties of the outer membrane, the integrity of the cytoplasmic membrane as well as the activity of membrane-bound enzymes, and the integrity of ribosomes. The pressure-induced denaturation of membrane bound enzymes results in generation of reactive oxygen species and subsequent cell death caused by oxidative stress. Remarkably, pressure resistance at the single cell level relates to the disposition of misfolded proteins in inclusion bodies. While the pressure resistance E. coli can be manipulated by over-expression or deletion of (stress) proteins, the mechanisms of pressure resistance in wild type strains is multi-factorial and not fully understood. This review aims to provide an overview on mechanisms of pressure-mediated cell death in E. coli, and the use of this information for optimization of high pressure processing of foods.

No MeSH data available.


Related in: MedlinePlus

Pressure effects on the cytoplasmic membrane and membrane bound proteins in E. coli. (A) High pressure decreases lateral motion and induces phase transition in the phospholipid bilayers of E. coli, and promotes gelation of the membrane lipids (Pagan and Mackey, 2000; Winter, 2002; Mañas and Mackey, 2004). Pressure resistance is influenced by membrane fluidity and fatty acid composition (Casadei et al., 2002). Exponential phase cell are more sensitive to pressure when compared to stationary phase cells (Pagan and Mackey, 2000; Casadei et al., 2002). Stationary phase cell express cfa encoding for cyclopropane fatty acyl phospholipid synthase (CFA). CFA converts unsaturated fatty acids to cyclopropane fatty acids, which contribute to acid resistance (Brown et al., 1997; Grogan and Cronan, 1997) and pressure resistance in E. coli (Charoenwong et al., 2011). (B) Sublethal pressure inactivates acid resistance in E. coli. The glutamate decarboxylase system for acid resistance is more resistant to pressure than other acid resistance mechanisms, and glutamic acid decarboxylation improved the survival of E. coli during post-pressure acid challenge (Kilimann et al., 2005). (C) The accumulation of compatible solutes including glycine-betaine, choline and sucrose, and the synthesis of trehalose protects against pressure-induced cell death (Van Opstal et al., 2003; Molina-Höppner et al., 2004; Charoenwong et al., 2011); BetT, ProP, and ProU are the major transporters for compatible solutes in E. coli. Mutants that are defective in trehalose synthesis exhibit a reduced resistance to pressure (Charoenwong et al., 2011). (D) Pressure inactivates F0F1-ATPase, which causes disruption of the acid efflux system (Wouters et al., 1998).
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Figure 2: Pressure effects on the cytoplasmic membrane and membrane bound proteins in E. coli. (A) High pressure decreases lateral motion and induces phase transition in the phospholipid bilayers of E. coli, and promotes gelation of the membrane lipids (Pagan and Mackey, 2000; Winter, 2002; Mañas and Mackey, 2004). Pressure resistance is influenced by membrane fluidity and fatty acid composition (Casadei et al., 2002). Exponential phase cell are more sensitive to pressure when compared to stationary phase cells (Pagan and Mackey, 2000; Casadei et al., 2002). Stationary phase cell express cfa encoding for cyclopropane fatty acyl phospholipid synthase (CFA). CFA converts unsaturated fatty acids to cyclopropane fatty acids, which contribute to acid resistance (Brown et al., 1997; Grogan and Cronan, 1997) and pressure resistance in E. coli (Charoenwong et al., 2011). (B) Sublethal pressure inactivates acid resistance in E. coli. The glutamate decarboxylase system for acid resistance is more resistant to pressure than other acid resistance mechanisms, and glutamic acid decarboxylation improved the survival of E. coli during post-pressure acid challenge (Kilimann et al., 2005). (C) The accumulation of compatible solutes including glycine-betaine, choline and sucrose, and the synthesis of trehalose protects against pressure-induced cell death (Van Opstal et al., 2003; Molina-Höppner et al., 2004; Charoenwong et al., 2011); BetT, ProP, and ProU are the major transporters for compatible solutes in E. coli. Mutants that are defective in trehalose synthesis exhibit a reduced resistance to pressure (Charoenwong et al., 2011). (D) Pressure inactivates F0F1-ATPase, which causes disruption of the acid efflux system (Wouters et al., 1998).

Mentions: Bacterial membranes are among the most pressure sensitive targets in bacterial cells. An overview on pressure-mediated damage to the cytoplasmic membrane is provided in Figure 2. Pressure application induces a phase transition from the physiological, liquid-crystalline phase to the gel phase (Winter, 2002). The pressure-induced phase transition of the cytoplasmic membrane also inhibits membrane bound enzymes (Wouters et al., 1998) and dissipates the proton motive force (Molina-Gutierrez et al., 2002). The in vivo observation of pressure-induced membrane phase transitions was achieved in Lactobacillus plantarum and Lactococcus lactis (Molina-Gutierrez et al., 2002; Ulmer et al., 2002) but not in E. coli, where observations of phase transitions of the cytoplasmic membrane are confounded by the outer membrane. The rapid dissipation of the proton motive force by pressure, however, was confirmed in E coli by in situ observation of the pH-dependent GFP fluorescence (Kilimann et al., 2005). Pressure as low as 10 MPa inhibits motility and substrate transport in E. coli (Bartlett, 2002). Remarkably, transport enzymes that are related to pH homeostasis of E. coli exhibit a differential resistance to pressure. Treatment of E. coli with 300 MPa inactivated arginine- and glucose dependent pH homeostasis but not the glutamate decarboxylase system (Figure 2; Kilimann et al., 2005). Pressure resistance is influenced by membrane fluidity and fatty acid composition (Casadei et al., 2002). Exponential phase cell are more sensitive to pressure when compared to stationary phase cells (Pagan and Mackey, 2000; Casadei et al., 2002). Stationary phase cells of E. coli convert unsaturated membrane lipids to cyclopropane fatty acids (Brown et al., 1997; Grogan and Cronan, 1997). Stationary phase cells also have a higher degree of crosslinking among membrane proteins and are less prone to lateral phase transition (Mirelman and Siegel, 1979; Souzu, 1986). Disruption of the cyclopropane fatty acid synthase has a decisive influence on the pressure resistance of E. coli (Charoenwong et al., 2011), confirming the prominent role of membrane properties in pressure-mediated cell death.


Mechanisms of pressure-mediated cell death and injury in Escherichia coli: from fundamentals to food applications.

Gänzle M, Liu Y - Front Microbiol (2015)

Pressure effects on the cytoplasmic membrane and membrane bound proteins in E. coli. (A) High pressure decreases lateral motion and induces phase transition in the phospholipid bilayers of E. coli, and promotes gelation of the membrane lipids (Pagan and Mackey, 2000; Winter, 2002; Mañas and Mackey, 2004). Pressure resistance is influenced by membrane fluidity and fatty acid composition (Casadei et al., 2002). Exponential phase cell are more sensitive to pressure when compared to stationary phase cells (Pagan and Mackey, 2000; Casadei et al., 2002). Stationary phase cell express cfa encoding for cyclopropane fatty acyl phospholipid synthase (CFA). CFA converts unsaturated fatty acids to cyclopropane fatty acids, which contribute to acid resistance (Brown et al., 1997; Grogan and Cronan, 1997) and pressure resistance in E. coli (Charoenwong et al., 2011). (B) Sublethal pressure inactivates acid resistance in E. coli. The glutamate decarboxylase system for acid resistance is more resistant to pressure than other acid resistance mechanisms, and glutamic acid decarboxylation improved the survival of E. coli during post-pressure acid challenge (Kilimann et al., 2005). (C) The accumulation of compatible solutes including glycine-betaine, choline and sucrose, and the synthesis of trehalose protects against pressure-induced cell death (Van Opstal et al., 2003; Molina-Höppner et al., 2004; Charoenwong et al., 2011); BetT, ProP, and ProU are the major transporters for compatible solutes in E. coli. Mutants that are defective in trehalose synthesis exhibit a reduced resistance to pressure (Charoenwong et al., 2011). (D) Pressure inactivates F0F1-ATPase, which causes disruption of the acid efflux system (Wouters et al., 1998).
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Related In: Results  -  Collection

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Figure 2: Pressure effects on the cytoplasmic membrane and membrane bound proteins in E. coli. (A) High pressure decreases lateral motion and induces phase transition in the phospholipid bilayers of E. coli, and promotes gelation of the membrane lipids (Pagan and Mackey, 2000; Winter, 2002; Mañas and Mackey, 2004). Pressure resistance is influenced by membrane fluidity and fatty acid composition (Casadei et al., 2002). Exponential phase cell are more sensitive to pressure when compared to stationary phase cells (Pagan and Mackey, 2000; Casadei et al., 2002). Stationary phase cell express cfa encoding for cyclopropane fatty acyl phospholipid synthase (CFA). CFA converts unsaturated fatty acids to cyclopropane fatty acids, which contribute to acid resistance (Brown et al., 1997; Grogan and Cronan, 1997) and pressure resistance in E. coli (Charoenwong et al., 2011). (B) Sublethal pressure inactivates acid resistance in E. coli. The glutamate decarboxylase system for acid resistance is more resistant to pressure than other acid resistance mechanisms, and glutamic acid decarboxylation improved the survival of E. coli during post-pressure acid challenge (Kilimann et al., 2005). (C) The accumulation of compatible solutes including glycine-betaine, choline and sucrose, and the synthesis of trehalose protects against pressure-induced cell death (Van Opstal et al., 2003; Molina-Höppner et al., 2004; Charoenwong et al., 2011); BetT, ProP, and ProU are the major transporters for compatible solutes in E. coli. Mutants that are defective in trehalose synthesis exhibit a reduced resistance to pressure (Charoenwong et al., 2011). (D) Pressure inactivates F0F1-ATPase, which causes disruption of the acid efflux system (Wouters et al., 1998).
Mentions: Bacterial membranes are among the most pressure sensitive targets in bacterial cells. An overview on pressure-mediated damage to the cytoplasmic membrane is provided in Figure 2. Pressure application induces a phase transition from the physiological, liquid-crystalline phase to the gel phase (Winter, 2002). The pressure-induced phase transition of the cytoplasmic membrane also inhibits membrane bound enzymes (Wouters et al., 1998) and dissipates the proton motive force (Molina-Gutierrez et al., 2002). The in vivo observation of pressure-induced membrane phase transitions was achieved in Lactobacillus plantarum and Lactococcus lactis (Molina-Gutierrez et al., 2002; Ulmer et al., 2002) but not in E. coli, where observations of phase transitions of the cytoplasmic membrane are confounded by the outer membrane. The rapid dissipation of the proton motive force by pressure, however, was confirmed in E coli by in situ observation of the pH-dependent GFP fluorescence (Kilimann et al., 2005). Pressure as low as 10 MPa inhibits motility and substrate transport in E. coli (Bartlett, 2002). Remarkably, transport enzymes that are related to pH homeostasis of E. coli exhibit a differential resistance to pressure. Treatment of E. coli with 300 MPa inactivated arginine- and glucose dependent pH homeostasis but not the glutamate decarboxylase system (Figure 2; Kilimann et al., 2005). Pressure resistance is influenced by membrane fluidity and fatty acid composition (Casadei et al., 2002). Exponential phase cell are more sensitive to pressure when compared to stationary phase cells (Pagan and Mackey, 2000; Casadei et al., 2002). Stationary phase cells of E. coli convert unsaturated membrane lipids to cyclopropane fatty acids (Brown et al., 1997; Grogan and Cronan, 1997). Stationary phase cells also have a higher degree of crosslinking among membrane proteins and are less prone to lateral phase transition (Mirelman and Siegel, 1979; Souzu, 1986). Disruption of the cyclopropane fatty acid synthase has a decisive influence on the pressure resistance of E. coli (Charoenwong et al., 2011), confirming the prominent role of membrane properties in pressure-mediated cell death.

Bottom Line: High hydrostatic pressure is commercially applied to extend the shelf life of foods, and to improve food safety.The targeted design of processes for the safe elimination of E. coli thus necessitates deeper insights into mechanisms of interaction and matrix-strain interactions.The pressure-induced denaturation of membrane bound enzymes results in generation of reactive oxygen species and subsequent cell death caused by oxidative stress.

View Article: PubMed Central - PubMed

Affiliation: Department of Agricultural, Food and Nutritional Science, University of Alberta , Edmonton, AB, Canada.

ABSTRACT
High hydrostatic pressure is commercially applied to extend the shelf life of foods, and to improve food safety. Current applications operate at ambient temperature and 600 MPa or less. However, bacteria that may resist this pressure level include the pathogens Staphylococcus aureus and strains of Escherichia coli, including shiga-toxin producing E. coli. The resistance of E. coli to pressure is variable between strains and highly dependent on the food matrix. The targeted design of processes for the safe elimination of E. coli thus necessitates deeper insights into mechanisms of interaction and matrix-strain interactions. Cellular targets of high pressure treatment in E. coli include the barrier properties of the outer membrane, the integrity of the cytoplasmic membrane as well as the activity of membrane-bound enzymes, and the integrity of ribosomes. The pressure-induced denaturation of membrane bound enzymes results in generation of reactive oxygen species and subsequent cell death caused by oxidative stress. Remarkably, pressure resistance at the single cell level relates to the disposition of misfolded proteins in inclusion bodies. While the pressure resistance E. coli can be manipulated by over-expression or deletion of (stress) proteins, the mechanisms of pressure resistance in wild type strains is multi-factorial and not fully understood. This review aims to provide an overview on mechanisms of pressure-mediated cell death in E. coli, and the use of this information for optimization of high pressure processing of foods.

No MeSH data available.


Related in: MedlinePlus