Performance of stress resistant variants of Listeria monocytogenes in mixed species biofilms with Lactobacillus plantarum

Metselaar, Karin I.; Ibusquiza, Paula Saá; Camargo, Angela Rocio Ortiz; Krieg, Myriam; Zwietering, Marcel H.; Besten, H.M.W. den; Abee, Tjakko

doi:10.1016/j.ijfoodmicro.2015.04.021

Cited by 14 publications

(7 citation statements)

References 35 publications

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“…Van Boeijen et al (11) reported that heat-resistant variants were not found after a single heat treatment due to the low probability of finding them due to their low prevalence, but after a few cycles, the fraction of heat-resistant variants increased significantly. Also the presence of L. monocytogenes in biofilms was shown to affect the stress resistance of the cells (19). It can be speculated that under more stringent heat treatment, the variant can become the dominating population and, with its slow growth, become a persister in industrial settings.…”

Section: Discussionmentioning

confidence: 99%

“…WT Listeria monocytogenes LO28 (Wageningen UR Food & Biobased Research, the Netherlands) and 8 of 23 acid-resistant variants isolated from the tail of this WT strain after acid exposure (9) were used in this study. The selected variants were 3, 7, 9, 12, 13, 14, 15, and 23, based on their genotypic and phenotypic characteristics representing different clusters (12,19). The stock cultures were kept in 15% (vol/vol) glycerol (Fluka) at Ϫ80°C, and before the experiments, cells from stock were grown for 2 days at 30°C on brain heart infusion (BHI; BD) agar plates.…”

Section: Methodsmentioning

confidence: 99%

“…Growth at mild pH stress can induce increased resistance to lethal acid stress but also to other stresses, like thermal stress (18). It was also shown that the different variants have different degrees of mild stress-adaptive behavior, affecting their stress resistance (19). The differences in behavior and resource allocation between the WT and variants might have consequences for their growth and survival under processing conditions.…”

mentioning

confidence: 99%

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Modeling and Validation of the Ecological Behavior of Wild-Type Listeria monocytogenes and Stress-Resistant Variants

Metselaar

Abee

Zwietering

et al. 2016

Appl Environ Microbiol

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Listeria monocytogenes exhibits a heterogeneous response upon stress exposure which can be partially attributed to the presence of stable stress-resistant variants. This study aimed to evaluate the impact of the presence of stress-resistant variants of Listeria monocytogenes and their corresponding trade-offs on population composition under different environmental conditions. A set of stress robustness and growth parameters of the wild type (WT) and an rpsU deletion variant was obtained and used to model their growth behavior under combined mild stress conditions and to model their kinetics under single-and mixed-strain conditions in a simulated food chain. Growth predictions for the WT and the rpsU deletion variant matched the experimental data generally well, although some deviations from the predictions were observed. The data highlighted the influence of the environmental conditions on the ratio between the WT and variant. Prediction of performance in the simulated food chain proved to be challenging. The trend of faster growth and lower stress robustness for the WT than for the rpsU variant in the different steps of the chain was confirmed, but especially for the inactivation steps and the time needed to resume growth after an inactivation step, the experimental data deviated from the model predictions. This report provides insights into the conditions which can select for stress-resistant variants in industrial settings and discusses their potential persistence in food processing environments. IMPORTANCEListeria monocytogenes exhibits a heterogeneous stress response which can partially be attributed to the presence of genetic variants. These stress-resistant variants survive better under severe conditions but have, on the other hand, a reduced growth rate. To date, the ecological behavior and potential impact of the presence of stress-resistant variants is not fully understood. In this study, we quantitatively assessed growth and inactivation behavior of wild-type L. monocytogenes and its stress-resistant variants. Predictions were validated under different conditions, as well as along a model food chain. This work illustrates the effects of environmental factors on population dynamics of L. monocytogenes and is a first step in evaluating the impact of population diversity on food safety. D iversity exists within bacterial populations which can, for example, be observed by tailing of inactivation curves upon stress exposure. This tail can be caused by either phenotypic or genotypic heterogeneity. Phenotypic heterogeneity refers to transiently increased resistance with a physiological or epigenetic background. Reasons for phenotypic heterogeneity can include the presence of persisters (1), bistability caused by noise in stochastic gene expression (2-4), or epigenetic phenotype switching (5). Genotypic heterogeneity refers to the presence of stable stressresistant variants with an inheritable stress-resistant phenotype caused by genomic alterations (6). These stable stress-resistant variants have bee...

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Modeling and Validation of the Ecological Behavior of Wild-Type Listeria monocytogenes and Stress-Resistant Variants

Metselaar

Abee

Zwietering

et al. 2016

Appl Environ Microbiol

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“…Taken together, biofilm-forming ability and LD 90 values underline the need to select different sanitizers, using rotating schemes, in order to prevent biocide resistance over time. Also, different strategies should be considered, other than the use of chemical biocides, as novel technologies, to control L. monocytogenes in the food production environment [ 60 , 61 ].…”

Section: Resultsmentioning

confidence: 99%

Genetic Subtyping, Biofilm-Forming Ability and Biocide Susceptibility of Listeria monocytogenes Strains Isolated from a Ready-to-Eat Food Industry

et al. 2020

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Listeria monocytogenes is a foodborne pathogen of special concern for ready-to-eat food producers. The control of its presence is a critical step in which food-grade sanitizers play an essential role. L. monocytogenes is believed to persist in food processing environments in biofilms, exhibiting less susceptibility to sanitizers than planktonic cells. This study aimed to test the susceptibility of L. monocytogenes in planktonic culture and biofilm to three commercial food-grade sanitizers and to benzalkonium chloride; together with the genetic subtyping of the isolates. L. monocytogenes isolates were collected from raw materials, final products and food-contact surfaces during a 6-year period from a ready-to-eat meat-producing food industry and genetically characterized. Serogrouping and pulsed-field gel electrophoresis (PFGE) revealed genetic variability and differentiated L. monocytogenes isolates in three clusters. The biofilm-forming ability assay revealed that the isolates were weak biofilm producers. L. monocytogenes strains were susceptible both in the planktonic and biofilm form to oxidizing and ethanol-based compounds and to benzalkonium chloride, but not to quaternary ammonium compound. A positive association of biofilm-forming ability and LD90 values for quaternary ammonium compound and benzalkonium chloride was found. This study highlights the need for preventive measures improvement and for a conscious selection and use of sanitizers in food-related environments to control Listeria monocytogenes.

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“…In some fermented food products, L. monocytogenes coexists with high levels of L. plantarum, and they have a similar niche. In the study of Metselaar et al (2015), L. monocytogenes acid-resistant variants could form mixed biofilms with L. plantarum, and an acidic environment created by homolactic fermentation of glucose by L. plantarum further increased the acid resistance of some variants. Microorganisms that improve biological adhesion and microbial coaggregation with other strains by secreting EPS or providing adhesion points and inducing them to colonize multispecies biofilms are referred to as bridging microorganisms (Rickard et al, 2003).…”

Section: 22mentioning

confidence: 99%

Multispecies biofilms in fermentation: Biofilm formation, microbial interactions, and communication

Yao

Hao

Zhou

et al. 2022

Comp Rev Food Sci Food Safe

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Food fermentation is driven by microorganisms, which usually coexist as multispecies biofilms. The activities and interactions of functional microorganisms and pathogenic bacteria in biofilms have important implications for the quality and safety of fermented foods. It was verified that the biofilm lifestyle benefited the fitness of microorganisms in harsh environments and intensified the cooperation and competition between biofilm members. This review focuses on multispecies biofilm formation, microbial interactions and communication in biofilms, and the application of multispecies biofilms in food fermentation. Microbial aggregation and adhesion are important steps in the early stage of multispecies biofilm formation. Different biofilm-forming abilities and strategies among microorganisms lead to several types of multispecies biofilm formation. The spatial distribution of multispecies biofilms reflects microbial interactions and biofilm function. Then, we discuss the intrinsic factors and external manifestations of multispecies biofilm system succession. Several typical interspecies cooperation and competition modes and mechanisms of microbial communication were reviewed in this review. The main limitations of the studies included in this review are the relatively small number of studies of biofilms formed by functional microorganisms during fermentation and the lack of direct evidence for the formation process of multispecies biofilms and microbial interactions and communication within biofilms. This review aims to provide the food industry with a sufficient understanding of multispecies biofilms in food fermentation.

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Performance of stress resistant variants of Listeria monocytogenes in mixed species biofilms with Lactobacillus plantarum

Cited by 14 publications

References 35 publications

Modeling and Validation of the Ecological Behavior of Wild-Type Listeria monocytogenes and Stress-Resistant Variants

Modeling and Validation of the Ecological Behavior of Wild-Type Listeria monocytogenes and Stress-Resistant Variants

Genetic Subtyping, Biofilm-Forming Ability and Biocide Susceptibility of Listeria monocytogenes Strains Isolated from a Ready-to-Eat Food Industry

Multispecies biofilms in fermentation: Biofilm formation, microbial interactions, and communication

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