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Metabolism and Physiology of Listeria monocytogenes

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Listeria monocytogenes: Pathogenesis and Host Response

Compared to the rich wealth of knowledge concerning the molecular basis of Listeria monocytogenes virulence, little is known on the physiological background necessary for allowing this facultative intracellular human pathogen to survive and replicate in its natural surroundings, particularly in the host cell’s cytosol. This cellular compartment appears to be the preferred site of replication, during a systemic infection caused by L. monocytogenes. Complementing earlier physiological studies, especially the more recent results obtained by comparative genomics, transcriptome, and proteome analyses, and by 13C-isotopolog perturbation studies, allow us today to draw a first (although still rather incomplete) picture of how the metabolism of these bacteria may function to facilitate efficient growth under extra- and intracellular conditions. In this chapter, we concentrate on the carbon- and nitrogen-metabolism of L. monocytogenes as deduced from these studies. Although many carbon- and nitrogen-metabolic pathways of L. monocytogenes appear to be similar to those of the extensively studied Bacillus subtilis, which like L. monocytogenes belongs to the group of low G+C gram-positive (Gp) bacteria, there seem to be some profound differences that are essential for understanding the interplay of the listerial metabolism with that of the host cells and hence may have an important impact on listerial virulence.

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References

  • Amezaga MR, Davidson I, McLaggan D, Verheul A, Abee T, and Booth IR (1995) The role of peptide metabolism in the growth of Listeria monocytogenes ATCC 23074 at high osmolarity. Microbiology 141 (Pt 1): 41–49.

    PubMed  CAS  Google Scholar 

  • Andersson U, Molenaar D, Radstrom P, and de Vos WM (2005) Unity in organisation and regulation of catabolic operons in Lactobacillus plantarum, Lactococcus lactis and Listeria monocytogenes. Syst Appl Microbiol 28: 187–195.

    Article  PubMed  CAS  Google Scholar 

  • Arcondeguy T, Jack R, and Merrick M (2001) P(II) signal transduction proteins, pivotal players in microbial nitrogen control. Microbiol Mol Biol Rev 65: 80–105.

    Article  PubMed  CAS  Google Scholar 

  • Begley M, Gahan CG, Kollas AK, Hintz M, Hill C, Jomaa H, and Eberl M (2004) The interplay between classical and alternative isoprenoid biosynthesis controls gammadelta T cell bioactivity of Listeria monocytogenes. FEBS Lett 561: 99–104.

    Article  PubMed  CAS  Google Scholar 

  • Behari J, and Youngman P (1998a) A homolog of CcpA mediates catabolite control in Listeria monocytogenes but not carbon source regulation of virulence genes. J Bacteriol 180: 6316–6324.

    CAS  Google Scholar 

  • Behari J, and Youngman P (1998b) Regulation of hly expression in Listeria monocytogenes by carbon sources and pH occurs through separate mechanisms mediated by PrfA. Infect Immun 66: 3635–3642.

    CAS  Google Scholar 

  • Blencke HM, Homuth G, Ludwig H, Mader U, Hecker M, and Stulke J (2003) Transcriptional profiling of gene expression in response to glucose inBacillus subtilis: regulation of the central metabolic pathways. Metab Eng 5: 133–149.

    Article  PubMed  CAS  Google Scholar 

  • Bradbeer C (1965) The clostridial fermentations of choline and ethanolamine. II. Requirement for a cobamide coenzyme by an ethanolamine deaminase. J Biol Chem 240: 4675–4681.

    PubMed  CAS  Google Scholar 

  • Buchrieser C, Rusniok C, Kunst F, Cossart P, and Glaser P (2003) Comparison of the genome sequences of Listeria monocytogenes and Listeria innocua: clues for evolution and pathogenicity. FEMS Immunol Med Microbiol 35:207–213.

    Article  PubMed  CAS  Google Scholar 

  • Buzolyova LS, and Somov GP (1999) Autotrophic assimilation of CO2 and C1-compounds by pathogenic bacteria. Biochemistry (Mosc) 64: 1146–1149.

    CAS  Google Scholar 

  • Chico-Calero I, Suarez M, Gonzalez-Zorn B, Scortti M, Slaghuis J, Goebel W, and Vazquez-Boland JA (2002) Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc Natl Acad Sci USA 99: 431–436.

    Article  PubMed  CAS  Google Scholar 

  • Christensen DP, and Hutkins RW (1994) Glucose uptake by Listeria monocytogenes Scott A and inhibition by pediocin JD. Appl Environ Microbiol 60: 3870–3873.

    PubMed  CAS  Google Scholar 

  • Collins MD, Wallbanks S, Lane DJ, Shah J, Nietupski R, Smida J, Dorsch M, and Stackebrandt E (1991) Phylogenetic analysis of the genus Listeria based on reverse transcriptase sequencing of 16S rRNA. Int J Syst Bacteriol 41: 240–246.

    Article  PubMed  CAS  Google Scholar 

  • Detsch C, and Stulke J (2003) Ammonium utilization in Bacillus subtilis: transport and regulatory functions of NrgA and NrgB. Microbiology 149: 3289–3297.

    Article  PubMed  CAS  Google Scholar 

  • Deutscher J, Kuster E, Bergstedt U, Charrier V, and Hillen W (1995) Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol Microbiol 15: 1049–1053.

    Article  PubMed  CAS  Google Scholar 

  • Dossonnet V, Monedero V, Zagorec M, Galinier A, Perez-Martinez G, and Deutscher J (2000) Phosphorylation of HPr by the bifunctional HPr Kinase/P-ser-HPr phosphatase from Lactobacillus casei controls catabolite repression and inducer exclusion but not inducer expulsion. J Bacteriol 182: 2582–2590.

    Article  PubMed  CAS  Google Scholar 

  • Eisenreich W, Slaghuis J, Laupitz R, Bussemer J, Stritzker J, Schwarz C, Schwarz R, Dandekar T, Bacher A, and Goebel W (2006) 13C Isotopolog perturbation studies of Listeria monocytogenes carbon metabolism and its modulation by the virulence regulator PrfA. Proc Nath Acad Sci USA 103: 2040–2045.

    Article  CAS  Google Scholar 

  • Fang FC, Libby SJ, Castor ME, and Fung AM (2005) Isocitrate lyase (AceA) is required for Salmonella persistence but not for acute lethal infection in mice. Infect Immun 73: 2547–2549.

    Article  PubMed  CAS  Google Scholar 

  • Farber JM, and Peterkin PI (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol Rev 55: 476–511.

    PubMed  CAS  Google Scholar 

  • Fieulaine S, Morera S, Poncet S, Mijakovic I, Galinier A, Janin J, Deutscher J, and Nessler S (2002) X-ray structure of a bifunctional protein kinase in complex with its protein substrate HPr. Proc Natl Acad Sci USA 99: 13437–13441.

    Article  PubMed  CAS  Google Scholar 

  • Fisher SH, and Magasanik B (1984) Synthesis of oxaloacetate in Bacillus subtilis mutants lacking the 2-ketoglutarate dehydrogenase enzymatic complex. J Bacteriol 158: 55–62.

    PubMed  CAS  Google Scholar 

  • Fisher SH (1999) Regulation of nitrogen metabolism in Bacillus subtilis: vive la difference! Mol Microbiol 32: 223–232.

    Article  PubMed  CAS  Google Scholar 

  • Friedman ME, and Roessler WG (1961) Growth of Listeria monocytogenes in defined media. J Bacteriol 82: 528–533.

    PubMed  CAS  Google Scholar 

  • Gahan CG, and Hill C (2005) Gastrointestinal phase of Listeria monocytogenes infection. J Appl Microbiol 98: 1345–1353.

    Article  PubMed  CAS  Google Scholar 

  • Galinier A, Kravanja M, Engelmann R, Hengstenberg W, Kilhoffer MC, Deutscher J, and Haiech J (1998) New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc Natl Acad Sci USA 95: 1823–1828.

    Article  PubMed  CAS  Google Scholar 

  • Glaser P, Frangeul L, Buchrieser C, Rusniok C, Amend A, Baquero F, Berche P, Bloecker H, Brandt P, Chakraborty T, Charbit A, Chetouani F, Couve E, de Daruvar A, Dehoux P, Domann E, Dominguez-Bernal G, Duchaud E, Durant L, Dussurget O, Entian KD, Fsihi H, Garcia-del Portillo F, Garrido P, Gautier L, Goebel W, Gomez-Lopez N, Hain T, Hauf J, Jackson D, Jones LM, Kaerst U, Kreft J, Kuhn M, Kunst F, Kurapkat G, Madueno E, Maitournam A, Vicente JM, Ng E, Nedjari H, Nordsiek G, Novella S, de Pablos B, Perez-Diaz JC, Purcell R, Remmel B, Rose M, Schlueter T, Simoes N, Tierrez A, Vazquez-Boland JA, Voss H, Wehland J, and Cossart P (2001) Comparative genomics of Listeria species. Science 294: 849–852.

    PubMed  CAS  Google Scholar 

  • Goetz M, Bubert A, Wang G, Chico-Calero I, Vazquez-Boland JA, Beck M, Slaghuis J, Szalay AA, and Goebel W (2001) Microinjection and growth of bacteria in the cytosol of mammalian host cells. Proc Natl Acad Sci USA 98: 12221–12226.

    Article  PubMed  CAS  Google Scholar 

  • Goldfine H, Johnston NC, and Knob C (1993) Nonspecific phospholipase C of Listeria monocytogenes: activity on phospholipids in Triton X-100-mixed micelles and in biological membranes. J Bacteriol 175: 4298–4306.

    PubMed  CAS  Google Scholar 

  • Gonzy-Treboul G, de Waard JH, Zagorec M, and Postma PW (1991) The glucose permease of the phosphotransferase system of Bacillus subtilis: evidence for IIGlc and IIIGlc domains. Mol Microbiol 5: 1241–1249.

    Article  PubMed  CAS  Google Scholar 

  • Gosseringer R, Kuster E, Galinier A, Deutscher J, and Hillen W (1997) Cooperative and non-cooperative DNA binding modes of catabolite control protein CcpA from Bacillus megaterium result from sensing two different signals. J Mol Biol 266: 665–676.

    Article  PubMed  CAS  Google Scholar 

  • Gottschalk G (1986) Bacterial Metabolism. New York: Springer-Verlag.

    Google Scholar 

  • Gray ML, and Killinger AH (1966) Listeria monocytogenes and listeric infections. Bacteriol Rev 30: 309–382.

    PubMed  CAS  Google Scholar 

  • Groves RD, and Welshimer HJ (1977) Separation of pathogenic from apathogenic Listeria monocytogenes by three in vitro reactions. J Clin Microbiol 5: 559–563.

    PubMed  CAS  Google Scholar 

  • Heller KB, Lin EC, and Wilson TH (1980) Substrate specificity and transport properties of the glycerol facilitator of Escherichia coli. J Bacteriol 144: 274–278.

    PubMed  CAS  Google Scholar 

  • Hueck CJ, and Hillen W (1995) Catabolite repression inBacillus subtilis: a global regulatory mechanism for the gram-positive bacteria? Mol Microbiol 15: 395–401.

    Article  PubMed  CAS  Google Scholar 

  • Jones BE, Dossonnet V, Kuster E, Hillen W, Deutscher J, and Klevit RE (1997) Binding of the catabolite repressor protein CcpA to its DNA target is regulated by phosphorylation of its corepressor HPr. J Biol Chem 272: 26530–26535.

    Article  PubMed  CAS  Google Scholar 

  • Jones CE, Shama G, Andrew PW, Roberts IS, and Jones D (1995) Comparative study of the growth of Listeria monocytogenes in defined media and demonstration of growth in continuous culture. J Appl Bacteriol 78: 66–70.

    PubMed  CAS  Google Scholar 

  • Joseph B, Przybilla K, Stühler C, Schauer K, Slaghuis J, Fuchs TM, and Goebel W (2006) Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J Bacteriol 188: 556–568.

    Article  PubMed  CAS  Google Scholar 

  • Karlin S, Theriot J, and Mrazek J (2004) Comparative analysis of gene expression among low G+C gram-positive genomes. Proc Natl Acad Sci USA 101: 6182–6187.

    Article  PubMed  CAS  Google Scholar 

  • Klarsfeld AD, Goossens PL, and Cossart P (1994) Five Listeria monocytogenes genes preferentially expressed in infected mammalian cells: plcA, purH, purD, pyrE and an arginine ABC transporter gene, arpJ. Mol Microbiol 13: 585–597.

    Article  PubMed  CAS  Google Scholar 

  • Kofoid E, Rappleye C, Stojiljkovic I, and Roth J (1999) The 17-gene ethanolamine (eut) operon of Salmonella typhimurium encodes five homologues of carboxysome shell proteins. J Bacteriol 181: 5317–5329.

    PubMed  CAS  Google Scholar 

  • Lin EC (1976) Glycerol dissimilation and its regulation in bacteria. Annu Rev Microbiol 30: 535–578.

    Article  PubMed  CAS  Google Scholar 

  • Marr AK, Joseph B, Mertins S, Ecke R, Müller-Altrock S, and Goebel W (2006) Overexpression of PrfA leads to growth inhibition of L. monocytogenes in glucose-containing culture media by interfering with glucose uptake. J Bacteriol 188: 3887–3901.

    Article  PubMed  CAS  Google Scholar 

  • Marquis H, Bouwer HG, Hinrichs DJ, and Portnoy DA (1993) Intracytoplasmic growth and virulence of Listeria monocytogenes auxotrophic mutants. Infect Immun 61: 3756–3760.

    PubMed  CAS  Google Scholar 

  • McKinney JD, Honer zu Bentrup K, Munoz-Elias EJ, Miczak A, Chen B, Chan WT, Swenson D, Sacchettini JC, Jacobs WR, Jr, and Russell DG (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735–738.

    Article  PubMed  CAS  Google Scholar 

  • Merrick MJ, and Edwards RA (1995) Nitrogen control in bacteria. Microbiol Rev 59: 604–622.

    PubMed  CAS  Google Scholar 

  • Mertins S, Joseph B, Goetz M, Ecke R, Seidel G, Sprehe M, Hillen W, Goebel W, and Müller-Altrock S (2007) Interference of PrfA with the carbohydrate catabolite repression (CCR) system in Listeria monocytogenes. J Bacteriol 189: 473–490.

    Article  PubMed  CAS  Google Scholar 

  • Milenbachs AA, Brown DP, Moors M, and Youngman P (1997) Carbon-source regulation of virulence gene expression in Listeria monocytogenes. Mol Microbiol 23: 1075–1085.

    Article  PubMed  CAS  Google Scholar 

  • Milenbachs Lukowiak A, Mueller KJ, Freitag NE, and Youngman P (2004) Deregulation of Listeria monocytogenes virulence gene expression by two distinct and semi-independent pathways. Microbiology 150: 321–333.

    Article  PubMed  CAS  Google Scholar 

  • Molle V, Nakaura Y, Shivers RP, Yamaguchi H, Losick R, Fujita Y, and Sonenshein AL (2003) Additional targets of the Bacillus subtilis global regulator CodY identified by chromatin immunoprecipitation and genome-wide transcript analysis. J Bacteriol 185: 1911–1922.

    Article  PubMed  CAS  Google Scholar 

  • Moreno MS, Schneider BL, Maile RR, Weyler W, and Saier MH, Jr (2001) Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol Microbiol 39: 1366–1381.

    Article  PubMed  CAS  Google Scholar 

  • Nichols DS, Presser KA, Olley J, Ross T, and McMeekin TA (2002) Variation of branched-chain fatty acids marks the normal physiological range for growth in Listeria monocytogenes. Appl Environ Microbiol 68: 2809–2813.

    Article  PubMed  CAS  Google Scholar 

  • O’Riordan M, Moors MA, and Portnoy DA (2003) Listeria intracellular growth and virulence require host-derived lipoic acid. Science 302: 462–464.

    Article  PubMed  CAS  Google Scholar 

  • Phan-Thanh L, and Gormon T (1997) A chemically defined minimal medium for the optimal culture of Listeria. Int J Food Microbiol 35: 91–95.

    Article  PubMed  CAS  Google Scholar 

  • Pine L, Malcolm GB, Brooks JB, and Daneshvar MI (1989) Physiological studies on the growth and utilization of sugars by Listeria species. Can J Microbiol 35: 245–254.

    Article  PubMed  CAS  Google Scholar 

  • Premaratne RJ, Lin WJ, and Johnson EA (1991) Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol 57: 3046–3048.

    PubMed  CAS  Google Scholar 

  • Reizer J, Saier MH, Jr, Deutscher J, Grenier F, Thompson J, and Hengstenberg W (1988) The phosphoenolpyruvate: sugar phosphotransferase system in gram-positive bacteria: properties, mechanism, and regulation. Crit Rev Microbiol 15: 297–338.

    Article  PubMed  CAS  Google Scholar 

  • Reizer J, Hoischen C, Titgemeyer F, Rivolta C, Rabus R, Stulke J, Karamata D, Saier MH, Jr, and Hillen W (1998) A novel protein kinase that controls carbon catabolite repression in bacteria. Mol Microbiol 27: 1157–1169.

    Article  PubMed  CAS  Google Scholar 

  • Romick TL, Fleming HP, and McFeeters RF (1996) Aerobic and anaerobic metabolism of Listeria monocytogenes in defined glucose medium. Appl Environ Microbiol 62: 304–307.

    PubMed  CAS  Google Scholar 

  • Romick TL, and Fleming HP (1998) Acetoin production as an indicator of growth and metabolic inhibition of Listeria monocytogenes. J Appl Microbiol 84: 18–24.

    Article  PubMed  CAS  Google Scholar 

  • Roof DM, and Roth JR (1988) Ethanolamine utilization in Salmonella typhimurium. J Bacteriol 170: 3855–3863.

    PubMed  CAS  Google Scholar 

  • Roof DM, and Roth JR (1989) Functions required for vitamin B12-dependent ethanolamine utilization in Salmonella typhimurium. J Bacteriol 171: 3316–3323.

    PubMed  CAS  Google Scholar 

  • Seeliger HP (1984) Modern taxonomy of the Listeria group relationship to its pathogenicity. Clin Invest Med 7: 217–221.

    PubMed  CAS  Google Scholar 

  • Seeliger HP, and Jones D (1986) Genus Listeria. In: Sneath PHA, Mair NS, Sharpe ME, and Holt JG (eds) Bergey’s manual of systematic bacteriology. Vol. 2. Baltimore, MD: Williams & Wilkins, pp. 1235–1245.

    Google Scholar 

  • Shivers RP, and Sonenshein AL (2005) Bacillus subtilis ilvB operon: an intersection of global regulons. Mol Microbiol 56: 1549–1559.

    Article  PubMed  CAS  Google Scholar 

  • Stritzker J, Janda J, Schoen C, Taupp M, Pilgrim S, Gentschev I, Schreier P, Geginat G, and Goebel W (2004) Growth, virulence, and immunogenicity of Listeria monocytogenes aro mutants. Infect Immun 72: 5622–5629.

    Article  PubMed  CAS  Google Scholar 

  • Titgemeyer F, and Hillen W (2002) Global control of sugar metabolism: a gram-positive solution. Antonie Van Leeuwenhoek 82: 59–71.

    Article  PubMed  CAS  Google Scholar 

  • Tojo S, Satomura T, Morisaki K, Deutscher J, Hirooka K, and Fujita Y (2005) Elaborate transcription regulation of the Bacillus subtilis ilv-leu operon involved in the biosynthesis of branched-chain amino acids through global regulators of CcpA, CodY and TnrA. Mol Microbiol 56: 1560–1573.

    Article  PubMed  CAS  Google Scholar 

  • Trivett TL, and Meyer EA (1971) Citrate cycle and related metabolism of Listeria monocytogenes. J Bacteriol 107: 770–779.

    PubMed  CAS  Google Scholar 

  • Tsai HN, and Hodgson DA (2003) Development of a synthetic minimal medium for Listeria monocytogenes. Appl Environ Microbiol 69: 6943–6945.

    Article  PubMed  CAS  Google Scholar 

  • Vadeboncoeur C, Frenette M, and Lortie LA (2000) Regulation of the pts operon in low G+C Gram-positive bacteria. J Mol Microbiol Biotechnol 2: 483–490.

    PubMed  CAS  Google Scholar 

  • Verheul A, Rombouts FM, and Abee T (1998) Utilization of oligopeptides by Listeria monocytogenes Scott A. Appl Environ Microbiol 64: 1059–1065.

    PubMed  CAS  Google Scholar 

  • Weickert MJ, and Chambliss GH (1990) Site-directed mutagenesis of a catabolite repression operator sequence in Bacillus subtilis. Proc Natl Acad Sci USA 87: 6238–6242.

    Article  PubMed  CAS  Google Scholar 

  • Weston LA, and Kadner RJ (1988) Role of uhp genes in expression of the Escherichia coli sugar-phosphate transport system. J Bacteriol 170: 3375–3383.

    PubMed  CAS  Google Scholar 

  • Wray LV, Jr, Ferson AE, Rohrer K, and Fisher SH (1996) TnrA, a transcription factor required for global nitrogen regulation in Bacillus subtilis. Proc Natl Acad Sci USA 93: 8841–8845.

    Article  PubMed  CAS  Google Scholar 

  • Yoshida K, Yamaguchi H, Kinehara M, Ohki YH, Nakaura Y, and Fujita Y (2003) Identification of additional TnrA-regulated genes of Bacillus subtilis associated with a TnrA box. Mol Microbiol 49: 157–165.

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Theodor-Boveri-Institut (Biozentrum), Lehrstuhl für Mikrobiologie, Universität Würzburg, D-97074 Würzburg, Germany

    Jörg Slaghuis, Biju Joseph & Werner Goebel

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  1. Jörg Slaghuis
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  2. Biju Joseph
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  1. Department of Microbiology, University of Pennsylvania, Philadelphia, PA, USA

    Howard Goldfine

  2. Department of Microbiology, University of Pennsylvania, Philadelphia, PA, USA

    Hao Shen

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Slaghuis, J., Joseph, B., Goebel, W. (2007). Metabolism and Physiology of Listeria monocytogenes. In: Goldfine, H., Shen, H. (eds) Listeria monocytogenes: Pathogenesis and Host Response. Springer, Boston, MA. https://doi.org/10.1007/978-0-387-49376-3_4

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