Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress

E S Giotis; I S Blair; D A McDowell

doi:10.1016/j.ijfoodmicro.2007.08.036

Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress

E S Giotis, I S Blair, D A McDowell

Biomedical Sciences Research

Research output: Contribution to journal › Article › peer-review

53 Citations (Scopus)

Abstract

Scanning electron microscopy (SEM) studies revealed that exposure to 4lethal alkaline stress induced statistically significant (P

Original language	English
Pages (from-to)	250-258
Journal	International Journal of Food Microbiology
Volume	120
Issue number	3
DOIs	https://doi.org/10.1016/j.ijfoodmicro.2007.08.036
Publication status	Published (in print/issue) - 2007

Bibliographical note

Reference text: Aldsworth, T.G., Sharman, R.L., Dodd, C.E.R., 1999. Bacterial suicide through stress. Cellular and Molecular Life Sciences 56, 378–383.
Becker, L.A., Cetin,M.S.,Hutkins, R.W., Benson,A.K., 1998. Identification of the gene encoding the alternative sigma factor σB from Listeria monocytogenes and its role in osmotolerance. Journal of Bacteriology 180, 4547–4554.
Becker, L.A., Evans, S.N., Hutkins, R.W., Benson, A.K., 2000. Role of σB in adaptation of Listeria monocytogenes to growth at low temperature. Journal of Bacteriology 182, 7083–7087.
Bennett, A.F., Lenski, R.E., Mittler, J.E., 1992. Evolutionary adaptation to temperature. Fitness responses of E. coli to changes in its thermal environments. Evolution 46, 16–30.
Bereksi, N., Gavini, F., Benezech, T., Faille, C., 2002. Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. Journal of Applied Microbiology 92, 556–565.
Brzin, B., 1973. The effect of NaCl on the morphology of Listeria monocytogenes. Zentralblatt fur Bakteriologie,Mikrobiologie und Hygiene. 1 Abt. Originale. B Hygiene 225, 80–84.
Brzin, B., 1975. Further observations of changed growth of Listeria monocytogenes on salt agar. Zentralblatt fur Bakteriologie, Mikrobiologie und Hygiene. 1 Abt. Originale. B Hygiene 232, 287–293.
Bubert, A., Riebe, J., Schnitzler, N., Schönberg, A., Goebel, W., Schubert, P., 1997. Isolation of catalase-negative Listeria monocytogenes strains from listeriosis patients and their rapid identification by anti-p60 antibodies and/or PCR. Journal of Clinical Microbiology 35, 179–183.
Butler, T., Frenck, R.W., Johnson, R.B., Khakhria, R., 2001. In vitro effects of azithromycin on Salmonella typhi: early inhibition by concentrations less than the MIC and reduction of MIC by alkaline pH and small inocula. Journal of Antimicrobial Chemotherapy 47, 455–458.
Chaturongakul, S., Boor, K.J., 2004. RsbT and RsbV contribute to σB dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Applied and Environmental Microbiology 70, 5349–5356.
Daskalov, H., Momfre, J., Sofos, J.N., 2006. Survival and growth of Listeria monocytogenes on sausage formulated with inoculated and stored rework product. Food Control 17, 981–986.
Dodd, C.E.R., Sharman, R.L., Bloomfield, S.F., Booth, I.R., Stewart, G.S.A.B., 1997. Inimical processes: bacterial self-destruction and sublethal injury. Trends in Food Science and Technology 8, 238–241.
Farber, J.M., Harwig, J., 1996. The Canadian position on Listeria monocytogenes in ready-to-eat foods. Food Control 7, 253–258.
Farber, J.M., Peterkin, P.I., 1991. Listeria monocytogenes, a food-borne pathogen. Microbiological Reviews 55, 476–511.
Ferreira, A., O'Byrne, C.P., Boor, K.J., 2001. Role of σB in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Applied and Environmental Microbiology 67, 4454–4457.
Ferreira, A., Sue, D., O'Byrne, C.P., Boor, K.J., 2003. Role of Listeria monocytogenes σB in survival of lethal acidic conditions and in the acquired acid tolerance response. Applied and Environmental Microbiology 69, 2692–2698.
Franco, C.M., Quinto, E.J., Fente, C., Rodriguez-Otero, J.L., Dominguez, L., Cepeda, A., 1995. Determination of the principal sources of Listeria monocytogenes contamination in poultry meat and poultry processing. Journal of Food Protection 58, 1320–1325.
Galdiero, G., D'Isanto, M., Aliberti, F., 1997. Effects of saline concentration, pH and growth temperature on the invasive capacity of Listeria monocytogenes. Research in Microbiology 148, 305–313.
Gardan, R., Cossart, P., Labadie, J., 2003. Identification of Listeria monocytogenes genes involved in salt and alkaline-pH tolerance. Applied and Environmental Microbiology 69, 3137–3143.
Guillier, L., Augustin, J.C., 2005. Influence of stress and growth conditions on individual lag time distributions of Listeria monocytogenes. Acta Horticulturae 674, 31–37.
Hahn, M.W., Moore, E.R.B., Hofle, M.G., 1999. Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Applied and Environmental Microbiology 65, 25–35.
Horner-Devine, M.C., Leibold, M.A., Smith, V.H., Bohannan, B.J.M., 2003. Bacterial diversity patterns along a gradient of primary productivity. Ecology Letters 6, 613–622.
Isom, L.L., Khambatta, Z.S., Moluf, J.L., Akers, D.F., Martin, S.E., 1995. Filament formation in Listeria monocytogenes. Journal of Food Protection 58, 1031–1033.
Jørgensen, F., Stephens, P.J., Knøchel, S., 1995. The effect of osmotic shock and subsequent adaptation on the thermotolerance and cell morphology of Listeria monocytogenes. Journal of Applied Microbiology 79, 274–281.
Jürgens, K., Sala, M.M., 2000. Predation-mediated shifts in size distribution of microbial biomass and activity during detritus decomposition. Oikos 91, 29–40.
Jydegaard-Axelsen, A.M., Aaes-Jørgensen, A., Koch, A.G., Jensen, J.S., Knøchel, S., 2005. Changes in growth, rRNA content, and cell morphology of Listeria monocytogenes induced by CO2 up- and downshift. International Journal of Food Microbiology 98, 145–155.
Kathariou, S., 2002. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. Journal of Food Protection 65, 1811–1829.
Li, J., Kolling, G.L., Matthews, K.R., Chikindas, M.L., 2003. Cold and carbon dioxide used as multi-hurdle preservation do not induce appearance of viable but non-culturable Listeria monocytogenes. Journal of Applied Microbiology 94, 48–53.
Liu, D., Lawrence, M.L., Ainsworth, A.J., Austin, F.W., 2005. Comparative assessment of acid, alkali and salt tolerance in Listeria monocytogenes virulent and avirulent strains. FEMS Microbiology Letters 243, 373–378.
Malits, A., Peters, F., Bayer-Giraldi, M., Marrase, C., Zoppini, A., Guadayol, O., Alcaraz, M., 2004. Effects of small-scale turbulence on bacteria: a matter of size. Microbial Ecology 48, 287–299.
Mattick, K.L., Phillips, L.E., Jørgensen, F., Lappin-Scott, H.M., Humphrey, T.J., 2003a. Filament formation by Salmonella spp. inoculated into liquid food matrices at refrigeration temperatures, and growth patterns when warmed. Journal of Food Protection 66, 215–219.
Mattick, K.L., Rowbury, R.J., Humphrey, T.J., 2003b. Morphological changes to Escherichia coli O157:H7, commensal E. coli and Salmonella spp. in response to marginal growth conditions, with special reference to mildly stressing temperatures. Science Progress 86, 103–113.
Maukonen, J., Matto, J., Wirtanen, G., Raaska, L., Mattila-Sandholm, T., Saarela, M., 2003. Methodologies for the characterization of microbes in industrial environments: a review. Journal of Industrial Microbiology and Biotechnology 30, 327–356.
Mendonca, A.F., Amoroso, T.L., Knabel, S.J., 1994. Destruction of gram-negative food-borne pathogens by high pH involves disruption of the cytoplasmic membrane. Applied and Environmental Microbiology 60, 4009–4014.
Minkowski, P., Staege, H., Groscurth, P., Schaffner, A., 2001. Effects of trimethoprim and co-trimoxazole on the morphology of Listeria monocytogenes in culture medium and after phagocytosis. Journal of Antimicrobial Chemotherapy 48, 185–193.
Neumann, G., Veeranagouda, Y., Karegoudar, T.B., Sahin, Ö., Mausezahl, I., Kabelitz, N., Kappelmeyer, U., Heipieper, H.J., 2005. Cells of Psuedomonas putida and Enterobacter spp. adapt to toxic organic compounds by increasing their size. Extremophiles 9, 163–168.
Nilsson, L., Chen, Y.H., Chikindas, M.L., Huss, H.H., Gram, L., Montville, T.J., 2000. Carbon dioxide and nisin act synergistically on Listeria monocytogenes. Applied and Environmental Microbiology 66, 769–774.
Nörrung, B., Andersen, J.K., Schlundt, J., 1999. Incidence and control of Listeria monocytogenes in foods in Denmark. International Journal of Food Microbiology 53, 195–203.
Ritz, M., Tholozan, J.L., Federighi, M., Pilet, M.F., 2001. Morphological and physiological characterisation of Listeria monocytogenes subjected to high hydrostatic pressure. Applied and Environmental Microbiology 67, 2240–2247.
Rowan, N.J., 1999. Evidence that inimical food-preservation barriers alter microbial resistance, cell morphology and virulence. Trends in Food Science and Technology 10, 261–270.
Rowan, N.J., Anderson, J.G., 1998. Effects of above-optimum growth temperature and cell morphology on thermotolerance of Listeria monocytogenes cells suspended in bovine milk. Applied and Environmental Microbiology 64, 2065–2071.
Rowan, N.J., Anderson, J.G., Candlish, A.A.G., 2000a. Cellular morphology of rough forms of Listeria monocytogenes isolated from clinical and food samples. Letters in Applied Microbiology 31, 319–322.
Rowan, N.J., Candlish, A.A.G., Bubert, A., Anderson, J.G., Kramer, K., McLauchlin, J., 2000b. Virulent rough filaments of Listeria monocytogenes from clinical and food samples secreting wild-type levels of cell-free p60 protein. Journal of Clinical Microbiology 38, 2643–2648.
Rowbury, R.J., Lazim, Z., Goodson, M., 1996. Regulatory aspects of alkali tolerance induction in Escherichia coli. Letters in Applied Microbiology 22, 429–432.
Segal, A.W., Geisow, M., Garcia, R., Harper, A., Miller, R., 1981. The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH. Nature 290, 406–409.
Shank, F.R., Elliot, E.L.,Wachsmuth, I.K., Losikoff, M.E., 1996. US position on Listeria monocytogenes in foods. Food Control 7, 229–234.
Sharma, M., Taormina, P.J., Beuchat, L.R., 2003. Habituation of foodborne pathogens exposed to extreme pH conditions: genetic basis and implications in foods and food processing environments. Food Science and Technology Research 9, 115–127.
Shi, B.H., Xia, X.H., 2003. Morphological changes of Pseudomonas pseudoalcaligenes in response to temperature selection. Current Microbiology 46, 120–123.
Taormina, P.J., Beuchat, L.R., 2001. Survival and heat resistance of Listeria monocytogenes after exposure to alkali and chlorine. Applied and Environmental Microbiology 67, 2555–2563.
Taormina, P.J., Beuchat, L.R., 2002a. Survival and growth of alkali-stressed Listeria monocytogenes on beef frankfurters and thermotolerance in frankfurter exudates. Journal of Food Protection 65, 291–298.
Taormina, P.J., Beuchat, L.R., 2002b. Survival of Listeria monocytogenes in commercial food-processing equipment cleaning solutions and subsequent sensitivity to sanitizers and heat. Journal of Applied Microbiology 92, 71–80.
Trusca, D., Scott, S., Thompson, C., Bramhill, D., 1998. Bacterial SOS checkpoint protein SulA inhibits polymerisation of purified FtsZ cell division protein. Journal of Bacteriology 180, 3946–3953.
Vasseur, C., Rigaud, N., Hebraud, M., Labadie, J., 2001. Combined effects of NaCl, NaOH, and biocides (monolaurin or lauric acid) on inactivation of Listeria monocytogenes and Pseudomonas spp. Journal of Food Protection 64, 1442–1445.
Vázquez-Boland, J.A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez- Bernal, G., Goebel, W., GonŸalez-Zorn, B., Wehland, J., Kreft, J., 2001. Listeria pathogenesis and molecular virulence determinants. Clinical Microbiology Reviews 14, 584–640.
Veeranagouda, Y., Karegoudar, T.B., Neumann, G., Heipieper, H.J., 2006. Enterobacter spp. VLGH12 growing in n-butanol as the sole carbon source and cells to which the alcohol is added as pure toxin show considerable differences in their adaptive responses. FEMS Microbiology Letters 254, 48–54.
Walk, G.C., 1996. The SOS response of E. coli. In: Neidhart, F.C., Reznikoff, W.S., Riley, M., Schaechter, M., Umbarger, H.E. (Eds.), Escherichia coli and Salmonella. ASM Press, Washington, pp. 1400–1416.
Wang, S.-Y., Hitchin, A.D., 1994. Enrichment of severely and moderately heat injured Listeria monocytogenes cells. Journal of Food Safety 14, 259–271.
Wemekamp-Kamphuis, H.H., Wouters, J.A., de Leeuw, P.P.L.A., Hain, T., Chakraborty, T., Abee, T., 2004. Identification of σB controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Applied and Environmental Microbiology 70, 3457–3466.
Wiedmann, M., Arvik, T.J., Hurley, R.J., Boor, K.J., 1998. General stress transcription factor σB and its role in acid tolerance and virulence of Listeria monocytogenes. Journal of Bacteriology 180, 3650–3656

Keywords

listeria monocytogenes
alkali
shape
sublethal stress
high hydrostatic-pressure
cell morphology
filament formation
growth temperature
escherichia-coli
carbon-dioxide
acid tolerance
food samples
survival
ph

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10.1016/j.ijfoodmicro.2007.08.036

http://uir.ulster.ac.uk/27624/1/Giotis-2007-Morphological_change.pdf

Cite this

@article{b745adcc7091423d90e377d70c805e84,

title = "Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress",

abstract = "Scanning electron microscopy (SEM) studies revealed that exposure to 4lethal alkaline stress induced statistically significant (P",

keywords = "listeria monocytogenes, alkali, shape, sublethal stress, high hydrostatic-pressure, cell morphology, filament formation, growth temperature, escherichia-coli, carbon-dioxide, acid tolerance, food samples, survival, ph",

author = "Giotis, {E S} and Blair, {I S} and McDowell, {D A}",

note = "Reference text: Aldsworth, T.G., Sharman, R.L., Dodd, C.E.R., 1999. Bacterial suicide through stress. Cellular and Molecular Life Sciences 56, 378–383. Becker, L.A., Cetin,M.S.,Hutkins, R.W., Benson,A.K., 1998. Identification of the gene encoding the alternative sigma factor σB from Listeria monocytogenes and its role in osmotolerance. Journal of Bacteriology 180, 4547–4554. Becker, L.A., Evans, S.N., Hutkins, R.W., Benson, A.K., 2000. Role of σB in adaptation of Listeria monocytogenes to growth at low temperature. Journal of Bacteriology 182, 7083–7087. Bennett, A.F., Lenski, R.E., Mittler, J.E., 1992. Evolutionary adaptation to temperature. Fitness responses of E. coli to changes in its thermal environments. Evolution 46, 16–30. Bereksi, N., Gavini, F., Benezech, T., Faille, C., 2002. Growth, morphology and surface properties of Listeria monocytogenes Scott A and LO28 under saline and acid environments. Journal of Applied Microbiology 92, 556–565. Brzin, B., 1973. The effect of NaCl on the morphology of Listeria monocytogenes. Zentralblatt fur Bakteriologie,Mikrobiologie und Hygiene. 1 Abt. Originale. B Hygiene 225, 80–84. Brzin, B., 1975. Further observations of changed growth of Listeria monocytogenes on salt agar. Zentralblatt fur Bakteriologie, Mikrobiologie und Hygiene. 1 Abt. Originale. B Hygiene 232, 287–293. Bubert, A., Riebe, J., Schnitzler, N., Sch{\"o}nberg, A., Goebel, W., Schubert, P., 1997. Isolation of catalase-negative Listeria monocytogenes strains from listeriosis patients and their rapid identification by anti-p60 antibodies and/or PCR. Journal of Clinical Microbiology 35, 179–183. Butler, T., Frenck, R.W., Johnson, R.B., Khakhria, R., 2001. In vitro effects of azithromycin on Salmonella typhi: early inhibition by concentrations less than the MIC and reduction of MIC by alkaline pH and small inocula. Journal of Antimicrobial Chemotherapy 47, 455–458. Chaturongakul, S., Boor, K.J., 2004. RsbT and RsbV contribute to σB dependent survival under environmental, energy, and intracellular stress conditions in Listeria monocytogenes. Applied and Environmental Microbiology 70, 5349–5356. Daskalov, H., Momfre, J., Sofos, J.N., 2006. Survival and growth of Listeria monocytogenes on sausage formulated with inoculated and stored rework product. Food Control 17, 981–986. Dodd, C.E.R., Sharman, R.L., Bloomfield, S.F., Booth, I.R., Stewart, G.S.A.B., 1997. Inimical processes: bacterial self-destruction and sublethal injury. Trends in Food Science and Technology 8, 238–241. Farber, J.M., Harwig, J., 1996. The Canadian position on Listeria monocytogenes in ready-to-eat foods. Food Control 7, 253–258. Farber, J.M., Peterkin, P.I., 1991. Listeria monocytogenes, a food-borne pathogen. Microbiological Reviews 55, 476–511. Ferreira, A., O'Byrne, C.P., Boor, K.J., 2001. Role of σB in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Applied and Environmental Microbiology 67, 4454–4457. Ferreira, A., Sue, D., O'Byrne, C.P., Boor, K.J., 2003. Role of Listeria monocytogenes σB in survival of lethal acidic conditions and in the acquired acid tolerance response. Applied and Environmental Microbiology 69, 2692–2698. Franco, C.M., Quinto, E.J., Fente, C., Rodriguez-Otero, J.L., Dominguez, L., Cepeda, A., 1995. Determination of the principal sources of Listeria monocytogenes contamination in poultry meat and poultry processing. Journal of Food Protection 58, 1320–1325. Galdiero, G., D'Isanto, M., Aliberti, F., 1997. Effects of saline concentration, pH and growth temperature on the invasive capacity of Listeria monocytogenes. Research in Microbiology 148, 305–313. Gardan, R., Cossart, P., Labadie, J., 2003. Identification of Listeria monocytogenes genes involved in salt and alkaline-pH tolerance. Applied and Environmental Microbiology 69, 3137–3143. Guillier, L., Augustin, J.C., 2005. Influence of stress and growth conditions on individual lag time distributions of Listeria monocytogenes. Acta Horticulturae 674, 31–37. Hahn, M.W., Moore, E.R.B., Hofle, M.G., 1999. Bacterial filament formation, a defense mechanism against flagellate grazing, is growth rate controlled in bacteria of different phyla. Applied and Environmental Microbiology 65, 25–35. Horner-Devine, M.C., Leibold, M.A., Smith, V.H., Bohannan, B.J.M., 2003. Bacterial diversity patterns along a gradient of primary productivity. Ecology Letters 6, 613–622. Isom, L.L., Khambatta, Z.S., Moluf, J.L., Akers, D.F., Martin, S.E., 1995. Filament formation in Listeria monocytogenes. Journal of Food Protection 58, 1031–1033. J{\o}rgensen, F., Stephens, P.J., Kn{\o}chel, S., 1995. The effect of osmotic shock and subsequent adaptation on the thermotolerance and cell morphology of Listeria monocytogenes. Journal of Applied Microbiology 79, 274–281. J{\"u}rgens, K., Sala, M.M., 2000. Predation-mediated shifts in size distribution of microbial biomass and activity during detritus decomposition. Oikos 91, 29–40. Jydegaard-Axelsen, A.M., Aaes-J{\o}rgensen, A., Koch, A.G., Jensen, J.S., Kn{\o}chel, S., 2005. Changes in growth, rRNA content, and cell morphology of Listeria monocytogenes induced by CO2 up- and downshift. International Journal of Food Microbiology 98, 145–155. Kathariou, S., 2002. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. Journal of Food Protection 65, 1811–1829. Li, J., Kolling, G.L., Matthews, K.R., Chikindas, M.L., 2003. Cold and carbon dioxide used as multi-hurdle preservation do not induce appearance of viable but non-culturable Listeria monocytogenes. Journal of Applied Microbiology 94, 48–53. Liu, D., Lawrence, M.L., Ainsworth, A.J., Austin, F.W., 2005. Comparative assessment of acid, alkali and salt tolerance in Listeria monocytogenes virulent and avirulent strains. FEMS Microbiology Letters 243, 373–378. Malits, A., Peters, F., Bayer-Giraldi, M., Marrase, C., Zoppini, A., Guadayol, O., Alcaraz, M., 2004. Effects of small-scale turbulence on bacteria: a matter of size. Microbial Ecology 48, 287–299. Mattick, K.L., Phillips, L.E., J{\o}rgensen, F., Lappin-Scott, H.M., Humphrey, T.J., 2003a. Filament formation by Salmonella spp. inoculated into liquid food matrices at refrigeration temperatures, and growth patterns when warmed. Journal of Food Protection 66, 215–219. Mattick, K.L., Rowbury, R.J., Humphrey, T.J., 2003b. Morphological changes to Escherichia coli O157:H7, commensal E. coli and Salmonella spp. in response to marginal growth conditions, with special reference to mildly stressing temperatures. Science Progress 86, 103–113. Maukonen, J., Matto, J., Wirtanen, G., Raaska, L., Mattila-Sandholm, T., Saarela, M., 2003. Methodologies for the characterization of microbes in industrial environments: a review. Journal of Industrial Microbiology and Biotechnology 30, 327–356. Mendonca, A.F., Amoroso, T.L., Knabel, S.J., 1994. Destruction of gram-negative food-borne pathogens by high pH involves disruption of the cytoplasmic membrane. Applied and Environmental Microbiology 60, 4009–4014. Minkowski, P., Staege, H., Groscurth, P., Schaffner, A., 2001. Effects of trimethoprim and co-trimoxazole on the morphology of Listeria monocytogenes in culture medium and after phagocytosis. Journal of Antimicrobial Chemotherapy 48, 185–193. Neumann, G., Veeranagouda, Y., Karegoudar, T.B., Sahin, {\"O}., Mausezahl, I., Kabelitz, N., Kappelmeyer, U., Heipieper, H.J., 2005. Cells of Psuedomonas putida and Enterobacter spp. adapt to toxic organic compounds by increasing their size. Extremophiles 9, 163–168. Nilsson, L., Chen, Y.H., Chikindas, M.L., Huss, H.H., Gram, L., Montville, T.J., 2000. Carbon dioxide and nisin act synergistically on Listeria monocytogenes. Applied and Environmental Microbiology 66, 769–774. N{\"o}rrung, B., Andersen, J.K., Schlundt, J., 1999. Incidence and control of Listeria monocytogenes in foods in Denmark. International Journal of Food Microbiology 53, 195–203. Ritz, M., Tholozan, J.L., Federighi, M., Pilet, M.F., 2001. Morphological and physiological characterisation of Listeria monocytogenes subjected to high hydrostatic pressure. Applied and Environmental Microbiology 67, 2240–2247. Rowan, N.J., 1999. Evidence that inimical food-preservation barriers alter microbial resistance, cell morphology and virulence. Trends in Food Science and Technology 10, 261–270. Rowan, N.J., Anderson, J.G., 1998. Effects of above-optimum growth temperature and cell morphology on thermotolerance of Listeria monocytogenes cells suspended in bovine milk. Applied and Environmental Microbiology 64, 2065–2071. Rowan, N.J., Anderson, J.G., Candlish, A.A.G., 2000a. Cellular morphology of rough forms of Listeria monocytogenes isolated from clinical and food samples. Letters in Applied Microbiology 31, 319–322. Rowan, N.J., Candlish, A.A.G., Bubert, A., Anderson, J.G., Kramer, K., McLauchlin, J., 2000b. Virulent rough filaments of Listeria monocytogenes from clinical and food samples secreting wild-type levels of cell-free p60 protein. Journal of Clinical Microbiology 38, 2643–2648. Rowbury, R.J., Lazim, Z., Goodson, M., 1996. Regulatory aspects of alkali tolerance induction in Escherichia coli. Letters in Applied Microbiology 22, 429–432. Segal, A.W., Geisow, M., Garcia, R., Harper, A., Miller, R., 1981. The respiratory burst of phagocytic cells is associated with a rise in vacuolar pH. Nature 290, 406–409. Shank, F.R., Elliot, E.L.,Wachsmuth, I.K., Losikoff, M.E., 1996. US position on Listeria monocytogenes in foods. Food Control 7, 229–234. Sharma, M., Taormina, P.J., Beuchat, L.R., 2003. Habituation of foodborne pathogens exposed to extreme pH conditions: genetic basis and implications in foods and food processing environments. Food Science and Technology Research 9, 115–127. Shi, B.H., Xia, X.H., 2003. Morphological changes of Pseudomonas pseudoalcaligenes in response to temperature selection. Current Microbiology 46, 120–123. Taormina, P.J., Beuchat, L.R., 2001. Survival and heat resistance of Listeria monocytogenes after exposure to alkali and chlorine. Applied and Environmental Microbiology 67, 2555–2563. Taormina, P.J., Beuchat, L.R., 2002a. Survival and growth of alkali-stressed Listeria monocytogenes on beef frankfurters and thermotolerance in frankfurter exudates. Journal of Food Protection 65, 291–298. Taormina, P.J., Beuchat, L.R., 2002b. Survival of Listeria monocytogenes in commercial food-processing equipment cleaning solutions and subsequent sensitivity to sanitizers and heat. Journal of Applied Microbiology 92, 71–80. Trusca, D., Scott, S., Thompson, C., Bramhill, D., 1998. Bacterial SOS checkpoint protein SulA inhibits polymerisation of purified FtsZ cell division protein. Journal of Bacteriology 180, 3946–3953. Vasseur, C., Rigaud, N., Hebraud, M., Labadie, J., 2001. Combined effects of NaCl, NaOH, and biocides (monolaurin or lauric acid) on inactivation of Listeria monocytogenes and Pseudomonas spp. Journal of Food Protection 64, 1442–1445. V{\'a}zquez-Boland, J.A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez- Bernal, G., Goebel, W., GonŸalez-Zorn, B., Wehland, J., Kreft, J., 2001. Listeria pathogenesis and molecular virulence determinants. Clinical Microbiology Reviews 14, 584–640. Veeranagouda, Y., Karegoudar, T.B., Neumann, G., Heipieper, H.J., 2006. Enterobacter spp. VLGH12 growing in n-butanol as the sole carbon source and cells to which the alcohol is added as pure toxin show considerable differences in their adaptive responses. FEMS Microbiology Letters 254, 48–54. Walk, G.C., 1996. The SOS response of E. coli. In: Neidhart, F.C., Reznikoff, W.S., Riley, M., Schaechter, M., Umbarger, H.E. (Eds.), Escherichia coli and Salmonella. ASM Press, Washington, pp. 1400–1416. Wang, S.-Y., Hitchin, A.D., 1994. Enrichment of severely and moderately heat injured Listeria monocytogenes cells. Journal of Food Safety 14, 259–271. Wemekamp-Kamphuis, H.H., Wouters, J.A., de Leeuw, P.P.L.A., Hain, T., Chakraborty, T., Abee, T., 2004. Identification of σB controlled genes and their impact on acid stress, high hydrostatic pressure, and freeze survival in Listeria monocytogenes EGD-e. Applied and Environmental Microbiology 70, 3457–3466. Wiedmann, M., Arvik, T.J., Hurley, R.J., Boor, K.J., 1998. General stress transcription factor σB and its role in acid tolerance and virulence of Listeria monocytogenes. Journal of Bacteriology 180, 3650–3656",

year = "2007",

doi = "10.1016/j.ijfoodmicro.2007.08.036",

language = "English",

volume = "120",

pages = "250--258",

journal = "International Journal of Food Microbiology",

publisher = "Elsevier",

number = "3",

}

TY - JOUR

T1 - Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress

AU - Giotis, E S

AU - Blair, I S

AU - McDowell, D A

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PY - 2007

Y1 - 2007

N2 - Scanning electron microscopy (SEM) studies revealed that exposure to 4lethal alkaline stress induced statistically significant (P

AB - Scanning electron microscopy (SEM) studies revealed that exposure to 4lethal alkaline stress induced statistically significant (P

KW - listeria monocytogenes

KW - alkali

KW - shape

KW - sublethal stress

KW - high hydrostatic-pressure

KW - cell morphology

KW - filament formation

KW - growth temperature

KW - escherichia-coli

KW - carbon-dioxide

KW - acid tolerance

KW - food samples

KW - survival

KW - ph

U2 - 10.1016/j.ijfoodmicro.2007.08.036

DO - 10.1016/j.ijfoodmicro.2007.08.036

M3 - Article

VL - 120

SP - 250

EP - 258

JO - International Journal of Food Microbiology

JF - International Journal of Food Microbiology

IS - 3

ER -

Morphological changes in Listeria monocytogenes subjected to sublethal alkaline stress

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