Transcriptomic and Phenotypic Responses of
            <i>Listeria monocytogenes</i>
            Strains Possessing Different Growth Efficiencies under Acidic Conditions

Bowman, John P.; Chang, Kim Jye Lee; Pinfold, Terry L.; Ross, Tom

doi:10.1128/aem.00315-10

Cited by 33 publications

(41 citation statements)

References 69 publications

(72 reference statements)

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“…Nevertheless, this potential cross-protective effect has not been assessed for other relevant food antimicrobial compounds. Further, the evidence of VirR regulon induction under acid stress prompted us to hypothesize that a potential cross-protective effect would be VirR mediated (43)(44)(45). Our results indicated that exposure to 2% PL increased subsequent NIS and EPL resistance of both the parent strain and the ⌬virR mutant.…”

Section: Figmentioning

confidence: 67%

“…In contrast, there have been reports of a cross-protective phenomenon, where prior exposure to a stress may increase resistance against a subsequent stress (20, 42). Additionally, acid-induced transcriptome profiling in L. monocytogenes has suggested upregulation of stress-and virulence-related genes, including the VirR regulon, as part of acid stress adaptation (43)(44)(45). To test the hypothesis that prior exposure to organic acids induces crossprotection against the selected antimicrobials and is mediated by VirR, we exposed the L. monocytogenes parent strain and H7858 ⌬virR to BHI (no acid control), 2% PL, and 0.14% SD, followed by subsequent challenge with antimicrobial compounds.…”

Section: Preexposure To Organic Acids Induces Cross-protection In Anmentioning

confidence: 99%

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VirR-Mediated Resistance of Listeria monocytogenes against Food Antimicrobials and Cross-Protection Induced by Exposure to Organic Acid Salts

Kang

Wiedmann

Boor

et al. 2015

Appl Environ Microbiol

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Formulations of ready-to-eat (RTE) foods with antimicrobial compounds constitute an important safety measure against foodborne pathogens such as Listeria monocytogenes. While the efficacy of many commercially available antimicrobial compounds has been demonstrated in a variety of foods, the current understanding of the resistance mechanisms employed by L. monocytogenes to counteract these stresses is limited. In this study, we screened in-frame deletion mutants of two-component system response regulators associated with the cell envelope stress response for increased sensitivity to commercially available antimicrobial compounds (nisin, lauric arginate, -polylysine, and chitosan). A virR deletion mutant showed increased sensitivity to all antimicrobials and significantly greater loss of membrane integrity when exposed to nisin, lauric arginate, or -polylysine (P < 0.05). The VirR-regulated operon, dltABCD, was shown to be the key contributor to resistance against these antimicrobial compounds, whereas another VirR-regulated gene, mprF, displayed an antimicrobial-specific contribution to resistance. An experiment with a ␤-glucuronidase (GUS) reporter fusion with the dlt promoter indicated that nisin does not specifically induce VirRdependent upregulation of dltABCD. Lastly, prior exposure of L. monocytogenes parent strain H7858 and the ⌬virR mutant to 2% potassium lactate enhanced subsequent resistance against nisin and -polylysine (P < 0.05). These data demonstrate that VirRS-mediated regulation of dltABCD is the major resistance mechanism used by L. monocytogenes against cell envelope-damaging food antimicrobials. Further, the potential for cross-protection induced by other food-related stresses (e.g., organic acids) needs to be considered when applying these novel food antimicrobials as a hurdle strategy for RTE foods. Control of Listeria monocytogenes in ready-to-eat (RTE) foods is an important food safety goal due to the high mortality rate associated with listeriosis, particularly in susceptible populations, such as pregnant women, the elderly, and those with a compromised immune system (1). L. monocytogenes is of particular concern for those RTE foods that support growth of this pathogen to high levels during refrigerated storage, which can potentially cause a life-threatening disease. L. monocytogenes harbors a variety of stress coping mechanisms that allow it to survive under suboptimal environmental conditions associated with foods (e.g., acidic, osmotic, and/or temperature stress) (2). The ability of L. monocytogenes to tolerate and grow under such a wide range of adverse conditions elevates the likelihood of foodborne transmission to a human host. Thus, a multipronged approach (e.g., prevention of postprocessing contamination and reformulation of RTE foods with antimicrobials) to limit L. monocytogenes in foods along the farm-to-fork continuum is critical to reduce the potential for foodborne illnesses involving this organism (3).Natural antimicrobials are commonly applied to RTE foods to control foodb...

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Section: Figmentioning

confidence: 67%

Section: Preexposure To Organic Acids Induces Cross-protection In Anmentioning

confidence: 99%

VirR-Mediated Resistance of Listeria monocytogenes against Food Antimicrobials and Cross-Protection Induced by Exposure to Organic Acid Salts

Kang

Wiedmann

Boor

et al. 2015

Appl Environ Microbiol

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“…Accumulation of intracellular ions is thought to have many growth-inhibiting effects, including reduction of the proton motive force, reduction of intracellular pH, interference with microbial metabolism, and anion toxicity (9,20,37). Bacteria respond to organic acid stress by transcriptional activation of the general stress (3,7) and oxidative stress (35) responses, membrane alterations (5) (possibly to reduce diffusion of organic acids or increase anion transport) (52), and metabolic changes (7,44,50). These organic acid responses appear to be distinct from the inorganic acid stress response caused by exposure to low pH from added HCl, which in L. monocytogenes includes activation of general stress responses, transcription of genes encoding proton pumps, and cell membrane modification (18,59).…”

mentioning

confidence: 99%

“…To date, acid stress response studies of bacteria have focused on acid-adapted exponential-phase (7,34) or stationary-phase (41) cells or on transcription differences during acid shock (exposures of less than 1 h) (3,5). As the end goal of bacteriostatic growth-inhibiting treatments in foods is to indefinitely extend the lag phase, our work focused specifically on the transcriptomic response to organic acid stress under conditions approximating adaptation (8 h into lag phase) during refrigerated storage (7°C, microaerophilic conditions) of a food product (pH 6.1, 4.65% water-phase [w.p.]…”

mentioning

confidence: 99%

The Transcriptional Response of Listeria monocytogenes during Adaptation to Growth on Lactate and Diacetate Includes Synergistic Changes That Increase Fermentative Acetoin Production

Stasiewicz

Wiedmann

Bergholz

2011

Appl Environ Microbiol

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The organic acids lactate and diacetate are commonly used in combination in ready-to-eat foods because they show synergistic ability to inhibit the growth of Listeria monocytogenes. Full-genome microarrays were used to investigate the synergistic transcriptomic responses of two L. monocytogenes strains, H7858 (serotype 4b) and F6854 (serotype 1/2a), to these two organic acids under conditions representing osmotic and cold stress encountered in foods. Strains were exposed to brain heart infusion (BHI) broth at 7°C with 4.65% water-phase (w.p.) NaCl at pH 6.1 with (i) 2% w.p. potassium lactate, (ii) 0.14% w.p. sodium diacetate, (iii) the combination of both at the same levels, or (iv) no organic acids as a control. RNA was extracted 8 h after exposure, during lag phase, to capture gene transcription changes during adaptation to the organic acid stress. Significant differential transcription of 1,041 genes in H7858 and 640 genes in F6854 was observed in at least one pair of the 4 different treatments. The effects of combined treatment with lactate and diacetate included (i) synergistic transcription differences for 474 and 209 genes in H7858 and F6854, respectively, (ii) differential transcription of genes encoding cation transporters and ABC transporters of metals, and (iii) altered metabolism, including induction of a nutrient-limiting stress response, reduction of menaquinone biosynthesis, and a shift from fermentative production of acetate and lactate to energetically less favorable, neutral acetoin. These data suggest that additional treatments that interfere with cellular energy generation processes could more efficiently inhibit the growth of L. monocytogenes.Listeria monocytogenes is a psychrotolerant food-borne pathogen that is of particular concern to the ready-to-eat-meat and -seafood industries because its ability to grow at temperatures as low as Ϫ0.4°C (70) reduces the ability of refrigeration to control the pathogen's growth in foods. Because L. monocytogenes generally contaminates foods at low levels (27) and has a high infectious dose (69), the ability of the organism to grow in foods is critical for its ability to cause disease (16). Foods do not support growth if they are stored frozen, have a pH of Յ4.4, have a water activity of Ͻ0.92, or incorporate some type of growth inhibiting measure (21), e.g., chemical preservatives (32). Ready-to-eat meat and seafood products have been identified as high-risk foods for listeriosis, as these foods support growth of L. monocytogenes (22), but it has also been predicted that reformulation of U.S. deli meats with effective growth inhibitors, e.g., the organic acids lactate and diacetate, would result in a 2-to 8-fold reduction of listeriosis due to consumption of these products (55). One particular advantage to using the combination of lactate and diacetate for L. monocytogenes control in meat and seafood products is that these inhibitors have been shown to have greater-than-additive, i.e., synergistic, growth-inhibiting effects (65), although the mechanisms...

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“…In addition several other putative cold, osmotic, acid and alkaline stress protection genes and proteins are known from gene expression analysis, which now allows rationalized creation of deletion mutants for functional studies ( Bowman et al, 2010;Chan et al, 2007;Giotis et al, 2008;Giotis et al, 2010;Liu et al, 2002). One of the putative cold adaptation genes identified in this bacterium is the lmo0501 locus of L. monocytogenes EGDe, which codes for the putative transcription activator protein Lmo0501.…”

Section: Introductionmentioning

confidence: 99%

The lmo0501 gene coding for a putative transcription activator protein in Listeria monocytogenes promotes growth under cold, osmotic and acid stress conditions

2011

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In L. monocytogenes EGDe, the lmo0501 gene locus encodes a protein similar to the mannitol transcription regulator (MltR) protein in B. subtilis and B. stearothermophilus. In this study we investigated its functional role in L. monocytogenes EGDe cells in view of growth under different stress conditions. Increased lmo0501 gene expression at mRNA level was detected in response to cold, osmotic and organic acid stress exposure. An EGDe Δlmo0501 mutant strain was diminished in growth compared to the wild type strain in minimal defined medium containing either glucose or fructose, as carbon sources. Furthermore the lmo0501 null mutant had retarded growth under cold (4°C), salt (NaCl) and organic acid stress conditions compared to the parental wild type strain. Our results confirm the role of the lmo0501 gene in view of adaptation of L. monocytogenes cells to stress conditions as well as a contribution to the efficient utilization of glucose and fructose as carbon sources.Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-60467 Originally published at: Michel, E. The lmo0501 gene coding for a putative transcription activator protein in Listeria monocytogenes promotes growth under cold, osmotic and acid stress conditions. 2011, University of Zurich, Vetsuisse Faculty.

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Transcriptomic and Phenotypic Responses of Listeria monocytogenes Strains Possessing Different Growth Efficiencies under Acidic Conditions

Cited by 33 publications

References 69 publications

VirR-Mediated Resistance of Listeria monocytogenes against Food Antimicrobials and Cross-Protection Induced by Exposure to Organic Acid Salts

VirR-Mediated Resistance of Listeria monocytogenes against Food Antimicrobials and Cross-Protection Induced by Exposure to Organic Acid Salts

The Transcriptional Response of Listeria monocytogenes during Adaptation to Growth on Lactate and Diacetate Includes Synergistic Changes That Increase Fermentative Acetoin Production

The lmo0501 gene coding for a putative transcription activator protein in Listeria monocytogenes promotes growth under cold, osmotic and acid stress conditions

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