Salt Stress Phenotypes in Listeria monocytogenes Vary by Genetic Lineage and Temperature
Publication: Foodborne Pathogens and Disease
Volume 7, Issue Number 12
Abstract
Listeria monocytogenes can survive and grow under wide-ranging environmental stress conditions encountered both in foods and in the host. The ability of certain L. monocytogenes subtypes to thrive under stress conditions present in specific niches was hypothesized to reflect genetic characteristics and phenotypic capabilities conserved among strains within a subtype. To quantify variations in salt stress phenotypes among 40 strains selected to represent the diversity of the three major L. monocytogenes genetic lineages and to determine if salt stress phenotypes were associated with genetic relatedness, we measured growth under salt stress at both 7°C and 37°C. At 7°C, in brain–heart infusion with 6% NaCl, average growth rates among the lineages were similar. A comparison of doubling times after exposure to salt stress at 7°C or 37°C indicated that growth at 7°C provided crossprotection to subsequent salt stress for strains in lineages I and II. At 37°C, in brain–heart infusion with 6% NaCl, lineage I and III strains grew significantly faster (p < 0.0001) than lineage II strains. Under salt stress at 37°C, differences in growth parameters were significantly (p < 0.005) associated with genetic relatedness of the strains. Compatible solute uptake is part of the L. monocytogenes salt stress response, but growth differences between the lineages were not related to differences in transcript levels of osmolyte transporter-encoding genes betL, gbuA, oppA, and opuCA. The combination of phylogenetic and phenotypic data suggests that L. monocytogenes lineage I and III strains, which are most commonly associated with human and animal disease, may be better adapted to osmotic stress at 37°C, conditions that are present in the host gastrointestinal tract.
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References
Angelidis ASSmith GM. Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined mediumAppl Environ Microbiol2003697492-7498. Angelidis AS and Smith GM. Role of the glycine betaine and carnitine transporters in adaptation of Listeria monocytogenes to chill stress in defined medium. Appl Environ Microbiol 2003;69:7492–7498.
Baranyi JRoberts TA. A dynamic approach to predicting bacterial growth in foodInt J Food Microbiol199423277-294. Baranyi J and Roberts TA. A dynamic approach to predicting bacterial growth in food. Int J Food Microbiol 1994;23:277–294.
Barbosa WBCabedo LWederquist HJSofos JNSchmidt GR. Growth variation among species and strains of Listeria in culture brothJ Food Prot199457765-769. Barbosa WB, Cabedo L, Wederquist HJ, Sofos JN, and Schmidt GR. Growth variation among species and strains of Listeria in culture broth. J Food Prot 1994;57:765–769.
Barmpalia-Davis IMGeornaras IKendall PASofos JN. Differences in survival among 13 Listeria monocytogenes strains in a dynamic model of the stomach and small intestineAppl Environ Microbiol2008745563-5567. Barmpalia-Davis IM, Geornaras I, Kendall PA, and Sofos JN. Differences in survival among 13 Listeria monocytogenes strains in a dynamic model of the stomach and small intestine. Appl Environ Microbiol 2008;74:5563–5567.
Bayles DOWilkinson BJ. Osmoprotectants and cryoprotectants for Listeria monocytogenesLett Appl Microbiol20003023-27. Bayles DO and Wilkinson BJ. Osmoprotectants and cryoprotectants for Listeria monocytogenes. Lett Appl Microbiol 2000;30:23–27.
Begley MGahan CGHill C. Bile stress response in Listeria monocytogenes LO28: adaptation, cross-protection, and identification of genetic loci involved in bile resistanceAppl Environ Microbiol2002686005-6012. Begley M, Gahan CG, and Hill C. Bile stress response in Listeria monocytogenes LO28: adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Appl Environ Microbiol 2002;68:6005–6012.
Begot CLebert ILebert A. Variability of the response of 66 Listeria monocytogenes and Listeria innocua strains to different growth conditionsFood Microbiol199714403-412. Begot C, Lebert I, and Lebert A. Variability of the response of 66 Listeria monocytogenes and Listeria innocua strains to different growth conditions. Food Microbiol 1997;14:403–412.
Bishop DKHinrichs DJ. Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirementsJ Immunol19871392005-2009. Bishop DK and Hinrichs DJ. Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J Immunol 1987;139:2005–2009.
Boerlin PPiffaretti JC. Typing of human, animal, food, and environmental isolates of Listeria monocytogenes by multilocus enzyme electrophoresisAppl Environ Microbiol1991571624-1629. Boerlin P and Piffaretti JC. Typing of human, animal, food, and environmental isolates of Listeria monocytogenes by multilocus enzyme electrophoresis. Appl Environ Microbiol 1991;57:1624–1629.
Borezee EPellegrini EBerche P. OppA of Listeria monocytogenes, an oligopeptide-binding protein required for bacterial growth at low temperature and involved in intracellular survivalInfect Immun2000687069-7077. Borezee E, Pellegrini E, and Berche P. OppA of Listeria monocytogenes, an oligopeptide-binding protein required for bacterial growth at low temperature and involved in intracellular survival. Infect Immun 2000;68:7069–7077.
Bruen TCPhilippe HBryant D. A simple and robust statistical test for detecting the presence of recombinationGenetics20061722665-2681. Bruen TC, Philippe H, and Bryant D. A simple and robust statistical test for detecting the presence of recombination. Genetics 2006;172:2665–2681.
Cai SKabuki DYKuaye AYCargioli TGChung MSNielsen RWiedmann M. Rational design of DNA sequence-based strategies for subtyping Listeria monocytogenesJ Clin Microbiol2002403319-3325. Cai S, Kabuki DY, Kuaye AY, Cargioli TG, Chung MS, Nielsen R, and Wiedmann M. Rational design of DNA sequence-based strategies for subtyping Listeria monocytogenes. J Clin Microbiol 2002;40:3319–3325.
Chen YHRoss WHGray MJWiedmann MWhiting RCScott VN. Attributing risk to Listeria monocytogenes subgroups: dose response in relation to genetic lineagesJ Food Prot200669335-344. Chen YH, Ross WH, Gray MJ, Wiedmann M, Whiting RC, and Scott VN. Attributing risk to Listeria monocytogenes subgroups: dose response in relation to genetic lineages. J Food Prot 2006;69:335–344.
De Jesus AJWhiting RC. Thermal inactivation, growth, and survival studies of Listeria monocytogenes strains belonging to three distinct genotypic lineagesJ Food Prot2003661611-1617. De Jesus AJ and Whiting RC. Thermal inactivation, growth, and survival studies of Listeria monocytogenes strains belonging to three distinct genotypic lineages. J Food Prot 2003;66:1611–1617.
den Bakker HCDidelot XFortes EDNightingale KKWiedmann M. Lineage specific recombination rates and microevolution in Listeria monocytogenesBMC Evol Biol20088277. den Bakker HC, Didelot X, Fortes ED, Nightingale KK, and Wiedmann M. Lineage specific recombination rates and microevolution in Listeria monocytogenes. BMC Evol Biol 2008;8:277.
Didelot XFalush D. Inference of bacterial microevolution using multilocus sequence dataGenetics20071751251-1266. Didelot X and Falush D. Inference of bacterial microevolution using multilocus sequence data. Genetics 2007;175:1251–1266.
Dykes GAMoorhead SM. Survival of osmotic and acid stress by Listeria monocytogenes strains of clinical or meat originInt J Food Microbiol200056161-166. Dykes GA and Moorhead SM. Survival of osmotic and acid stress by Listeria monocytogenes strains of clinical or meat origin. Int J Food Microbiol 2000;56:161–166.
[FDA] Food and Drug AdministrationListeria monocytogenes Risk Assessment2003www.fda.gov/Food/ScienceResearch/ResearchAreas/RiskAssessmentSafetyAssessment/ucm183966.htmFebruary12010. [FDA] Food and Drug Administration. Listeria monocytogenes Risk Assessment. 2003. Available at www.fda.gov/Food/ScienceResearch/ResearchAreas/RiskAssessmentSafetyAssessment/ucm183966.htm, accessed February 1, 2010.
Fisher MCBosch JYin ZStead DAWalker JSelway LBrown AJWalker LAGow NAStajich JEGarner TW. Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulenceMol Ecol200918415-429. Fisher MC, Bosch J, Yin Z, Stead DA, Walker J, Selway L, Brown AJ, Walker LA, Gow NA, Stajich JE, and Garner TW. Proteomic and phenotypic profiling of the amphibian pathogen Batrachochytrium dendrobatidis shows that genotype is linked to virulence. Mol Ecol 2009;18:415–429.
Fraser KRHarvie DCoote PJO'Byrne CP. Identification and characterization of an ATP binding cassette L-carnitine transporter in Listeria monocytogenesAppl Environ Microbiol2000664696-4704. Fraser KR, Harvie D, Coote PJ, and O'Byrne CP. Identification and characterization of an ATP binding cassette L-carnitine transporter in Listeria monocytogenes. Appl Environ Microbiol 2000;66:4696–4704.
Fugett EFortes ENnoka CWiedmann M. International Life Sciences Institute North America Listeria monocytogenes strain collection: development of standard Listeria monocytogenes strain sets for research and validation studiesJ Food Prot2006692929-2938. Fugett E, Fortes E, Nnoka C, and Wiedmann M. International Life Sciences Institute North America Listeria monocytogenes strain collection: development of standard Listeria monocytogenes strain sets for research and validation studies. J Food Prot 2006;69:2929–2938.
Gelman ARubin DB. Inference from iterative simulation using multiple sequencesStat Sci19927457-472. Gelman A and Rubin DB. Inference from iterative simulation using multiple sequences. Stat Sci 1992;7:457–472.
Geornaras ISkandamis PNBelk KEScanga JAKendall PASmith GCSofos JN. Post process control of Listeria monocytogenes on commercial frankfurters formulated with and without antimicrobials and stored at 10 degrees CJ Food Prot20066953-61. Geornaras I, Skandamis PN, Belk KE, Scanga JA, Kendall PA, Smith GC, and Sofos JN. Post process control of Listeria monocytogenes on commercial frankfurters formulated with and without antimicrobials and stored at 10 degrees C. J Food Prot 2006;69:53–61.
Gilbert RJMclauchlin JVelani SK. The contamination of pate by Listeria monocytogenes in England and Wales in 1989 and 1990Epidemiol Infect1993110543-551. Gilbert RJ, Mclauchlin J, and Velani SK. The contamination of pate by Listeria monocytogenes in England and Wales in 1989 and 1990. Epidemiol Infect 1993;110:543–551.
Gray MJZadoks RNFortes EDDogan BCai SChen YScott VNGombas DEBoor KJWiedmann M. Listeria monocytogenes isolates from foods and humans form distinct but overlapping populationsAppl Environ Microbiol2004705833-5841. Gray MJ, Zadoks RN, Fortes ED, Dogan B, Cai S, Chen Y, Scott VN, Gombas DE, Boor KJ, and Wiedmann M. Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl Environ Microbiol 2004;70:5833–5841.
Hahne HMader UOtto ABonn FSteil LBremer EHecker MBecher D. A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptationJ Bacteriol2010192870-882. Hahne H, Mader U, Otto A, Bonn F, Steil L, Bremer E, Hecker M, and Becher D. A comprehensive proteomics and transcriptomics analysis of Bacillus subtilis salt stress adaptation. J Bacteriol 2010;192:870–882.
Ho JLShands KNFriedland GEckind PFraser DW. An outbreak of type 4b Listeria monocytogenes infection involving patients from eight Boston hospitalsArch Intern Med1986146520-524. Ho JL, Shands KN, Friedland G, Eckind P, and Fraser DW. An outbreak of type 4b Listeria monocytogenes infection involving patients from eight Boston hospitals. Arch Intern Med 1986;146:520–524.
Hwang CASheen SJuneja VK. Effect of salt, smoke compound, and temperature on the survival of Listeria monocytogenes in Salmon during simulated smoking processesJ Food Sci200974M522-M529. Hwang CA, Sheen S, and Juneja VK. Effect of salt, smoke compound, and temperature on the survival of Listeria monocytogenes in Salmon during simulated smoking processes. J Food Sci 2009;74:M522–M529.
Ko RSmith LT. Identification of an ATP-driven, osmoregulated glycine betaine transport system in Listeria monocytogenesAppl Environ Microbiol1999654040-4048. Ko R and Smith LT. Identification of an ATP-driven, osmoregulated glycine betaine transport system in Listeria monocytogenes. Appl Environ Microbiol 1999;65:4040–4048.
Ko RSmith LTSmith GM. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenesJ Bacteriol1994176426-431. Ko R, Smith LT, and Smith GM. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J Bacteriol 1994;176:426–431.
Kvitek DJWill JLGasch AP. Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolatesPLoS Genet20084e1000223. Kvitek DJ, Will JL, and Gasch AP. Variations in stress sensitivity and genomic expression in diverse S. cerevisiae isolates. PLoS Genet 2008;4:e1000223.
Lianou AStopforth JDYoon YWiedmann MSofos JN. Growth and stress resistance variation in culture broth among Listeria monocytogenes strains of various serotypes and originsJ Food Prot2006692640-2647. Lianou A, Stopforth JD, Yoon Y, Wiedmann M, and Sofos JN. Growth and stress resistance variation in culture broth among Listeria monocytogenes strains of various serotypes and origins. J Food Prot 2006;69:2640–2647.
Nelson KEFouts DEMongodin EFRavel JDeBoy RTKolonay JFRasko DAAngiuoli SVGill SRPaulsen ITPeterson JWhite ONelson WCNierman WBeanan MJBrinkac LMDaugherty SCDodson RJDurkin ASMadupu RHaft DHSelengut JVan Aken SKhouri HFedorova NForberger HTran BKathariou SWonderling LDUhlich GABayles DOLuchansky JBFraser CM. Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this speciesNucleic Acids Res2004322386-2395. Nelson KE, Fouts DE, Mongodin EF, Ravel J, DeBoy RT, Kolonay JF, Rasko DA, Angiuoli SV, Gill SR, Paulsen IT, Peterson J, White O, Nelson WC, Nierman W, Beanan MJ, Brinkac LM, Daugherty SC, Dodson RJ, Durkin AS, Madupu R, Haft DH, Selengut J, Van Aken S, Khouri H, Fedorova N, Forberger H, Tran B, Kathariou S, Wonderling LD, Uhlich GA, Bayles DO, Luchansky JB, and Fraser CM. Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Res 2004;32:2386–2395.
Nightingale KBovell LGrajczyk AWiedmann M. Combined sigB allelic typing and multiplex PCR provide improved discriminatory power and reliability for Listeria monocytogenes molecular serotypingJ Microbiol Methods20076852-59. Nightingale K, Bovell L, Grajczyk A, and Wiedmann M. Combined sigB allelic typing and multiplex PCR provide improved discriminatory power and reliability for Listeria monocytogenes molecular serotyping. J Microbiol Methods 2007;68:52–59.
Nightingale KKLyles KAyodele MJalan PNielsen RWiedmann M. Novel method to identify source-associated phylogenetic clustering shows that Listeria monocytogenes includes niche-adapted clonal groups with distinct ecological preferencesJ Clin Microbiol2006443742-3751. Nightingale KK, Lyles K, Ayodele M, Jalan P, Nielsen R, and Wiedmann M. Novel method to identify source-associated phylogenetic clustering shows that Listeria monocytogenes includes niche-adapted clonal groups with distinct ecological preferences. J Clin Microbiol 2006;44:3742–3751.
Nightingale KKWindham KWiedmann M. Evolution and molecular phylogeny of Listeria monocytogenes isolated from human and animal listeriosis cases and foodsJ Bacteriol20051875537-5551. Nightingale KK, Windham K, and Wiedmann M. Evolution and molecular phylogeny of Listeria monocytogenes isolated from human and animal listeriosis cases and foods. J Bacteriol 2005;187:5537–5551.
Norton DMMcCamey MAGall KLScarlett JMBoor KJWiedmann M. Molecular studies on the ecology of Listeria monocytogenes in the smoked fish processing industryAppl Environ Microbiol200167198-205. Norton DM, McCamey MA, Gall KL, Scarlett JM, Boor KJ, and Wiedmann M. Molecular studies on the ecology of Listeria monocytogenes in the smoked fish processing industry. Appl Environ Microbiol 2001;67:198–205.
Nufer UStephan RTasara T. Growth characteristics of Listeria monocytogenes, Listeria welshimeri and Listeria innocua strains in broth cultures and a sliced bologna-type product at 4 and 7 degrees CFood Microbiol200724444-451. Nufer U, Stephan R, and Tasara T. Growth characteristics of Listeria monocytogenes, Listeria welshimeri and Listeria innocua strains in broth cultures and a sliced bologna-type product at 4 and 7 degrees C. Food Microbiol 2007;24:444–451.
Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCRNucleic Acids Res200129e45. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001;29:e45.
Pohl MAWiedmann MNightingale KK. Associations among Listeria monocytogenes genotypes and distinct clinical manifestations of listeriosis in cattleAm J Vet Res200667616-626. Pohl MA, Wiedmann M, and Nightingale KK. Associations among Listeria monocytogenes genotypes and distinct clinical manifestations of listeriosis in cattle. Am J Vet Res 2006;67:616–626.
Posada DCrandall KA. MODELTEST: testing the model of DNA substitutionBioinformatics199814817-818. Posada D and Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998;14:817–818.
Ragon MWirth THollandt FLavenir RLecuit MLe Monnier ABrisse S. A new perspective on Listeria monocytogenes evolutionPLoS Pathog20084e1000146. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M, Le Monnier A, and Brisse S. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 2008;4:e1000146.
Raimann ESchmid BStephan RTasara T. The alternative sigma factor sigma(L) of L. monocytogenes promotes growth under diverse environmental stressesFoodborne Pathog Dis20096583-591. Raimann E, Schmid B, Stephan R, and Tasara T. The alternative sigma factor sigma(L) of L. monocytogenes promotes growth under diverse environmental stresses. Foodborne Pathog Dis 2009;6:583–591.
Rasmussen OFSkouboe PDons LRossen LOlsen JE. Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genesMicrobiology1995141Pt 92053-2061. Rasmussen OF, Skouboe P, Dons L, Rossen L, and Olsen JE. Listeria monocytogenes exists in at least three evolutionary lines: evidence from flagellin, invasive associated protein and listeriolysin O genes. Microbiology 1995;141 (Pt 9):2053–2061.
Roberts ANightingale KJeffers GFortes EKongo JMWiedmann M. Genetic and phenotypic characterization of Listeria monocytogenes lineage IIIMicrobiology2006152685-693. Roberts A, Nightingale K, Jeffers G, Fortes E, Kongo JM, and Wiedmann M. Genetic and phenotypic characterization of Listeria monocytogenes lineage III. Microbiology 2006;152:685–693.
Ryser ET. Incidence and behavior of Listeria monocytogenes in cheese and other fermented dairy productsListeria, Listeriosis, and Food SafetyBoca RatonCRC Press2007405-502. Ryser ET. Incidence and behavior of Listeria monocytogenes in cheese and other fermented dairy products. In: Listeria, Listeriosis, and Food Safety. Boca Raton: CRC Press, 2007, pp. 405–502.
Sauders BDDurak MZFortes EWindham KSchukken YLembo AJ Jr.Akey BNightingale KKWiedmann M. Molecular characterization of Listeria monocytogenes from natural and urban environmentsJ Food Prot20066993-105. Sauders BD, Durak MZ, Fortes E, Windham K, Schukken Y, Lembo AJ, Jr., Akey B, Nightingale KK, and Wiedmann M. Molecular characterization of Listeria monocytogenes from natural and urban environments. J Food Prot 2006;69:93–105.
Sauders BDFortes EDMorse DLDumas NKiehlbauch JASchukken YHibbs JRWiedmann M. Molecular subtyping to detect human listeriosis clustersEmerg Infect Dis20039672-680. Sauders BD, Fortes ED, Morse DL, Dumas N, Kiehlbauch JA, Schukken Y, Hibbs JR, and Wiedmann M. Molecular subtyping to detect human listeriosis clusters. Emerg Infect Dis 2003;9:672–680.
Sauders BDMangione KVincent CSchermerhorn JFarchione CMDumas NBBopp DKornstein LFortes EDWindham KWiedmann M. Distribution of Listeria monocytogenes molecular subtypes among human and food isolates from New York State shows persistence of human disease-associated Listeria monocytogenes strains in retail environmentsJ Food Prot2004671417-1428. Sauders BD, Mangione K, Vincent C, Schermerhorn J, Farchione CM, Dumas NB, Bopp D, Kornstein L, Fortes ED, Windham K, and Wiedmann M. Distribution of Listeria monocytogenes molecular subtypes among human and food isolates from New York State shows persistence of human disease-associated Listeria monocytogenes strains in retail environments. J Food Prot 2004;67:1417–1428.
Sawyer S. Statistical tests for detecting gene conversionMol Biol Evol19896526-538. Sawyer S. Statistical tests for detecting gene conversion. Mol Biol Evol 1989;6:526–538.
Schmid BKlumpp JRaimann ELoessner MJStephan RTasara T. Role of cold shock proteins in growth of Listeria monocytogenes under cold and osmotic stress conditionsAppl Environ Microbiol2009751621-1627. Schmid B, Klumpp J, Raimann E, Loessner MJ, Stephan R, and Tasara T. Role of cold shock proteins in growth of Listeria monocytogenes under cold and osmotic stress conditions. Appl Environ Microbiol 2009;75:1621–1627.
Sleator RDClifford THill C. Gut osmolarity: A key environmental cue initiating the gastrointestinal phase of Listeria monocytogenes infection?Med Hypotheses2007691090-1092. Sleator RD, Clifford T, and Hill C. Gut osmolarity: A key environmental cue initiating the gastrointestinal phase of Listeria monocytogenes infection? Med Hypotheses 2007;69:1090–1092.
Sleator RDFrancis GAO'Beirne DGahan CGHill C. Betaine and carnitine uptake systems in Listeria monocytogenes affect growth and survival in foods and during infectionJ Appl Microbiol2003a95839-846. Sleator RD, Francis GA, O'Beirne D, Gahan CG, and Hill C. Betaine and carnitine uptake systems in Listeria monocytogenes affect growth and survival in foods and during infection. J Appl Microbiol 2003a;95:839–846.
Sleator RDGahan CGAbee THill C. Identification and disruption of BetL, a secondary glycine betaine transport system linked to the salt tolerance of Listeria monocytogenes LO28Appl Environ Microbiol1999652078-2083. Sleator RD, Gahan CG, Abee T, and Hill C. Identification and disruption of BetL, a secondary glycine betaine transport system linked to the salt tolerance of Listeria monocytogenes LO28. Appl Environ Microbiol 1999;65:2078–2083.
Sleator RDGahan CGHill C. A postgenomic appraisal of osmotolerance in Listeria monocytogenesAppl Environ Microbiol2003b691-9. Sleator RD, Gahan CG, and Hill C. A postgenomic appraisal of osmotolerance in Listeria monocytogenes. Appl Environ Microbiol 2003b;69:1–9.
Smith LT. Role of osmolytes in adaptation of osmotically stressed and chill-stressed Listeria monocytogenes grown in liquid media and on processed meat surfacesAppl Environ Microbiol1996623088-3093. Smith LT. Role of osmolytes in adaptation of osmotically stressed and chill-stressed Listeria monocytogenes grown in liquid media and on processed meat surfaces. Appl Environ Microbiol 1996;62:3088–3093.
Sue DFink DWiedmann MBoor KJ. sigmaB-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environmentMicrobiology20041503843-3855. Sue D, Fink D, Wiedmann M, and Boor KJ. sigmaB-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 2004;150:3843–3855.
Swaminathan BCabanes DZhang WCossart P. Listeria monocytogenesFood Microbiology: Fundamentals and FrontiersDoyle MPBeuchat LRWashington, DCASM Press2007457-491. Swaminathan B, Cabanes D, Zhang W, and Cossart P. Listeria monocytogenes. In: Food Microbiology: Fundamentals and Frontiers. Doyle MP and Beuchat LR. Washington, DC: ASM Press, 2007, pp. 457–491.
Tiganitas AZeaki NGounadaki ASDrosinos EHSkandamis PN. Study of the effect of lethal and sublethal pH and a(w) stresses on the inactivation or growth of Listeria monocytogenes and Salmonella TyphimuriumInt J Food Microbiol2009134104-112. Tiganitas A, Zeaki N, Gounadaki AS, Drosinos EH, and Skandamis PN. Study of the effect of lethal and sublethal pH and a(w) stresses on the inactivation or growth of Listeria monocytogenes and Salmonella Typhimurium. Int J Food Microbiol 2009;134:104–112.
Uyttendaele MRajkovic ABenos GFrancois KDevlieghere FDebevere J. Evaluation of a challenge testing protocol to assess the stability of ready-to-eat cooked meat products against growth of Listeria monocytogenesInt J Food Microbiol200490219-236. Uyttendaele M, Rajkovic A, Benos G, Francois K, Devlieghere F, and Debevere J. Evaluation of a challenge testing protocol to assess the stability of ready-to-eat cooked meat products against growth of Listeria monocytogenes. Int J Food Microbiol 2004;90:219–236.
van der Veen SMoezelaar RAbee TWells-Bennik MH. The growth limits of a large number of Listeria monocytogenes strains at combinations of stresses show serotype- and niche-specific traitsJ Appl Microbiol20081051246-1258. van der Veen S, Moezelaar R, Abee T, and Wells-Bennik MH. The growth limits of a large number of Listeria monocytogenes strains at combinations of stresses show serotype- and niche-specific traits. J Appl Microbiol 2008;105:1246–1258.
Vialette MPinon AChasseignaux ELange M. Growths kinetics comparison of clinical and seafood Listeria monocytogenes isolates in acid and osmotic environmentInt J Food Microbiol200382121-131. Vialette M, Pinon A, Chasseignaux E, and Lange M. Growths kinetics comparison of clinical and seafood Listeria monocytogenes isolates in acid and osmotic environment. Int J Food Microbiol 2003;82:121–131.
Vicente MFBaquero FPerezdiaz JC. Cloning and expression of the Listeria monocytogenes Hemolysin in Escherichia coliFEMS Microbiol Lett19853077-79. Vicente MF, Baquero F, and Perezdiaz JC. Cloning and expression of the Listeria monocytogenes Hemolysin in Escherichia coli. FEMS Microbiol Lett 1985;30:77–79.
Ward TJDucey TFUsgaard TDunn KABielawski JP. Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolatesAppl Environ Microbiol2008747629-7642. Ward TJ, Ducey TF, Usgaard T, Dunn KA, and Bielawski JP. Multilocus genotyping assays for single nucleotide polymorphism-based subtyping of Listeria monocytogenes isolates. Appl Environ Microbiol 2008;74:7629–7642.
Ward TJGorski LBorucki MKMandrell REHutchins JPupedis K. Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenesJ Bacteriol20041864994-5002. Ward TJ, Gorski L, Borucki MK, Mandrell RE, Hutchins J, and Pupedis K. Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. J Bacteriol 2004;186:4994–5002.
Wiedmann MBruce JLKeating CJohnson AEMcDonough PLBatt CA. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potentialInfect Immun1997652707-2716. Wiedmann M, Bruce JL, Keating C, Johnson AE, McDonough PL, and Batt CA. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect Immun 1997;65:2707–2716.
Wilgenbusch JCSwofford D. Inferring evolutionary trees with PAUP*Curr Protoc Bioinformatics2003Chapter 6:Unit 6 4. Wilgenbusch JC and Swofford D. Inferring evolutionary trees with PAUP*. Curr Protoc Bioinformatics 2003;Chapter 6:Unit 6 4.
Yang ZH. PAML 4: phylogenetic analysis by maximum likelihoodMol Biol Evol2007241586-1591. Yang ZH. PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007;24:1586–1591.
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Foodborne Pathogens and Disease
Volume 7 • Issue Number 12 • December 2010
Pages: 1537 - 1549
PubMed: 20707723
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Copyright 2010, Mary Ann Liebert, Inc.
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Published in print: December 2010
Published online: 1 December 2010
Published ahead of print: 14 August 2010
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