Internalization of Salmonella in Leafy Greens and Impact on Acid Tolerance

Salmonella colonizes the surface or the inner part of leafy greens, while the ability of internalized bacteria to evade common disinfection practices may pose a considerable risk. Hereby, we aimed to assess how the colonization and internalization of Salmonella spp. (i) vary with the type of leafy g...

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Veröffentlicht in:Applied and environmental microbiology 2022-03, Vol.88 (6), p.e0224921
Hauptverfasser: Grivokostopoulos, N C, Makariti, I P, Hilaj, N, Apostolidou, Z, Skandamis, P N
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container_start_page e0224921
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creator Grivokostopoulos, N C
Makariti, I P
Hilaj, N
Apostolidou, Z
Skandamis, P N
description Salmonella colonizes the surface or the inner part of leafy greens, while the ability of internalized bacteria to evade common disinfection practices may pose a considerable risk. Hereby, we aimed to assess how the colonization and internalization of Salmonella spp. (i) vary with the type of leafy green, the storage conditions (temperature, time), and Salmonella serovar at phenotypic and gene transcriptional level (regarding stress- and virulence- or type III secretion system [T3SS]-associated genes) and (ii) potentially impact the survival of the pathogen against subsequent exposure at lethal pH (2.7), mimicking the gastric acidity. Internalized Salmonella reached 3.0 to 5.0 log CFU/g depending on storage conditions and vegetable, with spinach and chicory allowing the highest ( 0.05) internalization. Prolonged storage (48 h) at 20°C increased the recovery of internalized Salmonella in spinach and green amaranth by 1.0 to 1.5 log units. Colonization of Salmonella on/in leafy vegetables induced the transcription (maximum fold change [FCmax], ∼2,000) of T3SS-related genes. Interserovar variation regarding the internalization ability of Salmonella was observed only in lettuce and green amaranth in a time- and temperature-dependent manner. Attached cells exhibited higher survival rates against low pH than the internalized subpopulation; however, habituation at 20°C in lettuce and amaranth induced acid tolerance to internalized cells, manifested by the 1.5 to 2.0 log CFU/g survivors after 75 min at pH 2.7. Habituation of Salmonella in vegetable extracts sensitized it toward acid, while indigenous microbiota had limited impact on acid resistance of the organism. These findings reveal physiological aspects of Salmonella colonizing leafy vegetables that could be useful in fresh produce microbial risk assessment. Consumption of leafy greens has been increasingly associated with foodborne illnesses, and their contamination could occur at pre- and/or postharvest level. Human pathogens may become passively or actively internalized in plant tissues, thereby escaping decontamination procedures. Plant colonization may impact bacterial physiology such as stress resistance and virulence. In this study, it was demonstrated that internalization of Salmonella spp., at the postharvest level, varied with type of vegetable, serovar, and storage conditions. Attached and internalized subpopulations of Salmonella on/in leafy greens showed distinct physiological responses regarding
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Hereby, we aimed to assess how the colonization and internalization of Salmonella spp. (i) vary with the type of leafy green, the storage conditions (temperature, time), and Salmonella serovar at phenotypic and gene transcriptional level (regarding stress- and virulence- or type III secretion system [T3SS]-associated genes) and (ii) potentially impact the survival of the pathogen against subsequent exposure at lethal pH (2.7), mimicking the gastric acidity. Internalized Salmonella reached 3.0 to 5.0 log CFU/g depending on storage conditions and vegetable, with spinach and chicory allowing the highest ( 0.05) internalization. Prolonged storage (48 h) at 20°C increased the recovery of internalized Salmonella in spinach and green amaranth by 1.0 to 1.5 log units. Colonization of Salmonella on/in leafy vegetables induced the transcription (maximum fold change [FCmax], ∼2,000) of T3SS-related genes. Interserovar variation regarding the internalization ability of Salmonella was observed only in lettuce and green amaranth in a time- and temperature-dependent manner. Attached cells exhibited higher survival rates against low pH than the internalized subpopulation; however, habituation at 20°C in lettuce and amaranth induced acid tolerance to internalized cells, manifested by the 1.5 to 2.0 log CFU/g survivors after 75 min at pH 2.7. Habituation of Salmonella in vegetable extracts sensitized it toward acid, while indigenous microbiota had limited impact on acid resistance of the organism. These findings reveal physiological aspects of Salmonella colonizing leafy vegetables that could be useful in fresh produce microbial risk assessment. Consumption of leafy greens has been increasingly associated with foodborne illnesses, and their contamination could occur at pre- and/or postharvest level. Human pathogens may become passively or actively internalized in plant tissues, thereby escaping decontamination procedures. Plant colonization may impact bacterial physiology such as stress resistance and virulence. In this study, it was demonstrated that internalization of Salmonella spp., at the postharvest level, varied with type of vegetable, serovar, and storage conditions. Attached and internalized subpopulations of Salmonella on/in leafy greens showed distinct physiological responses regarding transcriptional changes of stress- and virulence-associated genes, as well as survival capacity against subsequent exposure to lethal pH (2.7). 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Interserovar variation regarding the internalization ability of Salmonella was observed only in lettuce and green amaranth in a time- and temperature-dependent manner. Attached cells exhibited higher survival rates against low pH than the internalized subpopulation; however, habituation at 20°C in lettuce and amaranth induced acid tolerance to internalized cells, manifested by the 1.5 to 2.0 log CFU/g survivors after 75 min at pH 2.7. Habituation of Salmonella in vegetable extracts sensitized it toward acid, while indigenous microbiota had limited impact on acid resistance of the organism. These findings reveal physiological aspects of Salmonella colonizing leafy vegetables that could be useful in fresh produce microbial risk assessment. Consumption of leafy greens has been increasingly associated with foodborne illnesses, and their contamination could occur at pre- and/or postharvest level. 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Hereby, we aimed to assess how the colonization and internalization of Salmonella spp. (i) vary with the type of leafy green, the storage conditions (temperature, time), and Salmonella serovar at phenotypic and gene transcriptional level (regarding stress- and virulence- or type III secretion system [T3SS]-associated genes) and (ii) potentially impact the survival of the pathogen against subsequent exposure at lethal pH (2.7), mimicking the gastric acidity. Internalized Salmonella reached 3.0 to 5.0 log CFU/g depending on storage conditions and vegetable, with spinach and chicory allowing the highest ( 0.05) internalization. Prolonged storage (48 h) at 20°C increased the recovery of internalized Salmonella in spinach and green amaranth by 1.0 to 1.5 log units. Colonization of Salmonella on/in leafy vegetables induced the transcription (maximum fold change [FCmax], ∼2,000) of T3SS-related genes. Interserovar variation regarding the internalization ability of Salmonella was observed only in lettuce and green amaranth in a time- and temperature-dependent manner. Attached cells exhibited higher survival rates against low pH than the internalized subpopulation; however, habituation at 20°C in lettuce and amaranth induced acid tolerance to internalized cells, manifested by the 1.5 to 2.0 log CFU/g survivors after 75 min at pH 2.7. Habituation of Salmonella in vegetable extracts sensitized it toward acid, while indigenous microbiota had limited impact on acid resistance of the organism. These findings reveal physiological aspects of Salmonella colonizing leafy vegetables that could be useful in fresh produce microbial risk assessment. Consumption of leafy greens has been increasingly associated with foodborne illnesses, and their contamination could occur at pre- and/or postharvest level. 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source American Society for Microbiology; MEDLINE; PubMed Central; Alma/SFX Local Collection
subjects Acid resistance
Acidity
Acids
Amaranth
Colonization
Colony Count, Microbial
Disinfection
Food Contamination - analysis
Food Microbiology
Gastric juice
Genes
Habituation
Habituation (learning)
Humans
Internalization
Lactuca - microbiology
Microbiota
Microorganisms
Mimicry
pH effects
Plant Leaves - microbiology
Risk assessment
Salmonella
Salmonella - genetics
Spinach
Storage conditions
Survival
Temperature dependence
Transcription
Vegetables
Vegetables - microbiology
Virulence
title Internalization of Salmonella in Leafy Greens and Impact on Acid Tolerance
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