Carbon metabolism of intracellular bacterial pathogens and possible links to virulence

New technologies such as high-throughput methods and 13C-isotopologue-profiling analysis are beginning to provide us with insight into the in vivo metabolism of microorganisms, especially in the host cell compartments that are colonized by intracellular bacterial pathogens. In this Review, we discuss the recent progress made in determining the major carbon sources and metabolic pathways used by model intracellular bacterial pathogens that replicate either in the cytosol or in vacuoles of infected host cells. Furthermore, we highlight the possible links between intracellular carbon metabolism and the expression of virulence genes.

[1]  R. Schoenfeld,et al.  Comparative Genomics of Listeria Species , 1976 .

[2]  C. Haidaris,et al.  Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[3]  B. Stocker,et al.  Effect of different purine auxotrophic mutations on mouse-virulence of a Vi-positive strain of Salmonella dublin and of two strains of Salmonella typhimurium. , 1987, Microbial pathogenesis.

[4]  J. Maddox.  Maintaining the balance , 1988, Nature.

[5]  E. Johnson,et al.  Development of an improved chemically defined minimal medium for Listeria monocytogenes , 1991, Applied and environmental microbiology.

[6]  B. Finlay,et al.  Intracellular replication is essential for the virulence of Salmonella typhimurium. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[7]  A J Sinskey,et al.  Oxidized redox state of glutathione in the endoplasmic reticulum. , 1992, Science.

[8]  C. Cheeseman.  Role of intestinal basolateral membrane in absorption of nutrients. , 1992, The American journal of physiology.

[9]  H. Bouwer,et al.  Intracytoplasmic growth and virulence of Listeria monocytogenes auxotrophic mutants , 1993, Infection and immunity.

[10]  D. Loo,et al.  'Active' sugar transport in eukaryotes. , 1994, The Journal of experimental biology.

[11]  T. Szyperski.  Biosynthetically Directed Fractional 13C‐labeling of Proteinogenic Amino Acids , 1995 .

[12]  Catherine A. Lee,et al.  hilA is a novel ompR/toxR family member that activates the expression of Salmonella typhimurium invasion genes , 1995, Molecular microbiology.

[13]  T. Szyperski.  Biosynthetically directed fractional 13C-labeling of proteinogenic amino acids. An efficient analytical tool to investigate intermediary metabolism. , 1995, European journal of biochemistry.

[14]  M. Levine,et al.  Engineered deltaguaB-A deltavirG Shigella flexneri 2a strain CVD 1205: construction, safety, immunogenicity, and potential efficacy as a mucosal vaccine , 1996, Infection and immunity.

[15]  H. Holms,et al.  Flux analysis and control of the central metabolic pathways in Escherichia coli. , 1996, FEMS microbiology reviews.

[16]  W. Goebel,et al.  A new PrfA‐regulated gene of Listeria monocytogenes encoding a small, secreted protein which belongs to the family of internalins , 1996, Molecular microbiology.

[17]  G. Macfarlane,et al.  Human colonic microbiota: ecology, physiology and metabolic potential of intestinal bacteria. , 1997, Scandinavian journal of gastroenterology. Supplement.

[18]  S Falkow,et al.  Macrophage‐dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival , 1998, Molecular microbiology.

[19]  G. Micheli,et al.  A role for H-NS in the regulation of the virF gene of Shigella and enteroinvasive Escherichia coli. , 1998, Research in microbiology.

[20]  B. Barrell,et al.  Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence , 1998, Nature.

[21]  W. Eisenreich,et al.  Elucidation of novel biosynthetic pathways and metabolite flux patterns by retrobiosynthetic NMR analysis , 1998 .

[22]  P. Youngman,et al.  A homolog of CcpA mediates catabolite control in Listeria monocytogenes but not carbon source regulation of virulence genes. , 1998, Journal of bacteriology.

[23]  S. Fisher,et al.  Regulation of nitrogen metabolism in Bacillus subtilis: vive la différence! , 1999, Molecular microbiology.

[24]  J. van Reeuwijk,et al.  Salmonella SirA is a global regulator of genes mediating enteropathogenesis , 1999, Molecular Microbiology.

[25]  F. Fang,et al.  Cellular routes of invasion by enteropathogens. , 2000, Current opinion in microbiology.

[26]  S. Méresse,et al.  Salmonella maintains the integrity of its intracellular vacuole through the action of SifA , 2000, The EMBO journal.

[27]  P. Sansonetti,et al.  Bacterial signals and cell responses during Shigella entry into epithelial cells , 2000, Cellular microbiology.

[28]  James C. Sacchettini,et al.  Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase , 2000, Nature.

[29]  F. Heffron,et al.  Salmonella SsrB activates a global regulon of horizontally acquired genes , 2000, Molecular microbiology.

[30]  H. Smith,et al.  Questions about the behaviour of bacterial pathogens in vivo. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  W. Goebel,et al.  Hpt, a bacterial homolog of the microsomal glucose- 6-phosphate translocase, mediates rapid intracellular proliferation in Listeria , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[32]  W. Bishai,et al.  Regulation of virulence genes in Mycobacterium tuberculosis. , 2001, International journal of medical microbiology : IJMM.

[33]  L. Gautier,et al.  Comparative Genomics of Listeria Species , 2001, Science.

[34]  R. Wilson,et al.  Complete genome sequence of Salmonella enterica serovar Typhimurium LT2 , 2001, Nature.

[35]  M. Hensel,et al.  Salmonella pathogenicity islands encoding type III secretion systems. , 2001, Microbes and infection.

[36]  W. Goebel,et al.  Microinjection and growth of bacteria in the cytosol of mammalian host cells , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[37]  P. Ratcliffe,et al.  Activation of the HIF pathway in cancer. , 2001, Current opinion in genetics & development.

[38]  Russell Maurer,et al.  Intestinal short‐chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA , 2002, Molecular microbiology.

[39]  Adrian L. Harris,et al.  Hypoxia — a key regulatory factor in tumour growth , 2002, Nature Reviews Cancer.

[40]  S. Payne,et al.  Identification of Chromosomal Shigella flexneri Genes Induced by the Eukaryotic Intracellular Environment , 2002, Infection and Immunity.

[41]  Jie Dong,et al.  Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. , 2002, Nucleic acids research.

[42]  C. Beuzón,et al.  Growth and killing of a Salmonella enterica serovar Typhimurium sifA mutant strain in the cytosol of different host cell lines. , 2002, Microbiology.

[43]  J. Liautard,et al.  The intramacrophagic environment of Brucella suis and bacterial response. , 2002, Veterinary microbiology.

[44]  P. Cossart,et al.  An RNA Thermosensor Controls Expression of Virulence Genes in Listeria monocytogenes , 2002, Cell.

[45]  Christopher M. Sassetti,et al.  Genetic requirements for mycobacterial survival during infection , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[46]  D. Russell,et al.  pckA-deficient Mycobacterium bovis BCG shows attenuated virulence in mice and in macrophages. , 2003, Microbiology.

[47]  I. S. Wood,et al.  Glucose transporters (GLUT and SGLT): expanded families of sugar transport proteins , 2003, British Journal of Nutrition.

[48]  Arthur Thompson,et al.  Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica , 2002, Molecular microbiology.

[49]  D. Portnoy,et al.  Listeria Intracellular Growth and Virulence Require Host-Derived Lipoic Acid , 2003, Science.

[50]  C. Dorman,et al.  An extended role for the nucleoid structuring protein H‐NS in the virulence gene regulatory cascade of Shigella flexneri , 2003, Molecular microbiology.

[51]  U. Sauer,et al.  Metabolic flux profiling of Escherichia coli mutants in central carbon metabolism using GC-MS. , 2003, European journal of biochemistry.

[52]  G. Rossi,et al.  Analysis of Virulence and Inflammatory Potential of Shigella flexneri Purine Biosynthesis Mutants , 2003, Infection and Immunity.

[53]  Yang Liu,et al.  Transcriptional Adaptation of Mycobacterium tuberculosis within Macrophages , 2003, The Journal of experimental medicine.

[54]  Marcus Taupp,et al.  Growth, Virulence, and Immunogenicity of Listeria monocytogenes aro Mutants , 2004, Infection and Immunity.

[55]  J. Vázquez-Boland,et al.  Negative control of Listeria monocytogenes virulence genes by a diffusible autorepressor , 2004, Molecular microbiology.

[56]  Rick Lyons,et al.  The temporal expression profile of Mycobacterium tuberculosis infection in mice. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[57]  W. Goebel,et al.  Inefficient replication of Listeria innocua in the cytosol of mammalian cells. , 2004, The Journal of infectious diseases.

[58]  E. Rubin,et al.  Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Christoph Dehio,et al.  Signature-tagged mutagenesis: technical advances in a negative selection method for virulence gene identification. , 2005, Current opinion in microbiology.

[60]  Jens Nielsen,et al.  The next wave in metabolome analysis. , 2005, Trends in biotechnology.

[61]  Ferric C. Fang,et al.  Isocitrate Lyase (AceA) Is Required for Salmonella Persistence but Not for Acute Lethal Infection in Mice , 2005, Infection and Immunity.

[62]  A. Cataldi,et al.  Mutation in mce operons attenuates Mycobacterium tuberculosis virulence. , 2005, Microbes and infection.

[63]  Hong Liu,et al.  Transcriptional Adaptation of Shigella flexneri during Infection of Macrophages and Epithelial Cells: Insights into the Strategies of a Cytosolic Bacterial Pathogen , 2005, Infection and Immunity.

[64]  C. Altier.  Genetic and environmental control of salmonella invasion. , 2005, Journal of microbiology.

[65]  B. Jones.  Salmonella Invasion Gene Regulation , 2005 .

[66]  E. Muñoz-Elías,et al.  Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence , 2005, Nature Medicine.

[67]  B. Jones.  Salmonella invasion gene regulation: a story of environmental awareness. , 2005, Journal of microbiology.

[68]  P. Wheeler,et al.  The pyruvate requirement of some members of the Mycobacterium tuberculosis complex is due to an inactive pyruvate kinase: implications for in vivo growth , 2005, Molecular microbiology.

[69]  E. Denamur,et al.  Analysis of virulence plasmid gene expression defines three classes of effectors in the type III secretion system of Shigella flexneri. , 2005, Microbiology.

[70]  Clifton E. Barry,et al.  Tuberculosis — metabolism and respiration in the absence of growth , 2005, Nature Reviews Microbiology.

[71]  E. Muñoz-Elías,et al.  Role of the methylcitrate cycle in Mycobacterium tuberculosis metabolism, intracellular growth, and virulence , 2006, Molecular microbiology.

[72]  N. Casali,et al.  A phylogenomic analysis of the Actinomycetales mce operons , 2007, BMC Genomics.

[73]  James C Sacchettini,et al.  Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis , 2006, Molecular microbiology.

[74]  C. Francke,et al.  How Phosphotransferase System-Related Protein Phosphorylation Regulates Carbohydrate Metabolism in Bacteria , 2006, Microbiology and Molecular Biology Reviews.

[75]  Brunero Liseo,et al.  Profiling of Mycobacterium tuberculosis gene expression during human macrophage infection: upregulation of the alternative sigma factor G, a group of transcriptional regulators, and proteins with unknown function. , 2006, Research in microbiology.

[76]  C. Sasakawa,et al.  Intracellular survival of Shigella , 2006, Cellular microbiology.

[77]  U. Sauer,et al.  Article number: 62 REVIEW Metabolic networks in motion: 13 C-based flux analysis , 2022 .

[78]  E. Domann,et al.  Intracellular Gene Expression Profile of Listeria monocytogenes , 2006, Infection and Immunity.

[79]  A. Jansen,et al.  Differential gene expression of pathogens inside infected hosts. , 2006, Current opinion in microbiology.

[80]  T. Dandekar,et al.  13C isotopologue perturbation studies of Listeria monocytogenes carbon metabolism and its modulation by the virulence regulator PrfA , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[81]  W. Goebel,et al.  Identification of Listeria monocytogenes Genes Contributing to Intracellular Replication by Expression Profiling and Mutant Screening , 2006, Journal of bacteriology.

[82]  T. Conway,et al.  Role of Gluconeogenesis and the Tricarboxylic Acid Cycle in the Virulence of Salmonella enterica Serovar Typhimurium in BALB/c Mice , 2006, Infection and Immunity.

[83]  E. Muñoz-Elías,et al.  Carbon metabolism of intracellular bacteria , 2006, Cellular microbiology.

[84]  S. Fortune,et al.  Characterization of mycobacterial virulence genes through genetic interaction mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[85]  P. Mahadevan,et al.  An overview , 2007, Journal of Biosciences.

[86]  W. Goebel,et al.  Interference of Components of the Phosphoenolpyruvate Phosphotransferase System with the Central Virulence Gene Regulator PrfA of Listeria monocytogenes , 2006, Journal of bacteriology.

[87]  Study of the role of Mce3R on the transcription of mce genes of Mycobacterium tuberculosis , 2008, BMC Microbiology.

[88]  David G. Russell,et al.  Who puts the tubercle in tuberculosis? , 2007, Nature Reviews Microbiology.

[89]  A. Kolb,et al.  Interplay between CRP-cAMP and PII-Ntr systems forms novel regulatory network between carbon metabolism and nitrogen assimilation in Escherichia coli , 2007, Nucleic Acids Research.

[90]  M. Stevens,et al.  Raman microspectroscopy for non-invasive biochemical analysis of single cells. , 2007, Biochemical Society transactions.

[91]  J. Slauch,et al.  Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. , 2007, Current opinion in microbiology.

[92]  S. Rubino,et al.  SipA, SopA, SopB, SopD and SopE2 effector proteins of Salmonella enterica serovar Typhimurium are synthesized at late stages of infection in mice. , 2007, Microbiology.

[93]  J. Vázquez-Boland,et al.  The PrfA virulence regulon. , 2007, Microbes and infection.

[94]  W. Solbach,et al.  Chlamydia pneumoniae directly interferes with HIF‐1α stabilization in human host cells , 2007, Cellular microbiology.

[95]  P. Sansonetti,et al.  Shigella’s ways of manipulating the host intestinal innate and adaptive immune system: a tool box for survival? , 2007, Immunology and cell biology.

[96]  Dirk Bumann,et al.  Identification of host-induced pathogen genes by differential fluorescence induction reporter systems , 2007, Nature Protocols.

[97]  Peter J. Peters,et al.  M. tuberculosis and M. leprae Translocate from the Phagolysosome to the Cytosol in Myeloid Cells , 2007, Cell.

[98]  S. Johnston,et al.  Mycobacterial Bacilli Are Metabolically Active during Chronic Tuberculosis in Murine Lungs: Insights from Genome-Wide Transcriptional Profiling , 2007, Journal of bacteriology.

[99]  L. Dijkhuizen,et al.  A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages , 2007, Proceedings of the National Academy of Sciences.

[100]  W. Goebel,et al.  Life of Listeria monocytogenes in the host cells' cytosol. , 2007, Microbes and infection.

[101]  Ben Sidders,et al.  A highly conserved transcriptional repressor controls a large regulon involved in lipid degradation in Mycobacterium smegmatis and Mycobacterium tuberculosis , 2007, Molecular microbiology.

[102]  A. Keating,et al.  Functional properties and genomics of glucose transporters. , 2007, Current genomics.

[103]  A. Sonenshein,et al.  Control of key metabolic intersections in Bacillus subtilis , 2007, Nature Reviews Microbiology.

[104]  A. Bäumler,et al.  From bench to bedside: stealth of enteroinvasive pathogens , 2008, Nature Reviews Microbiology.

[105]  B. Görke,et al.  Carbon catabolite repression in bacteria: many ways to make the most out of nutrients , 2008, Nature Reviews Microbiology.

[106]  Jerry Kaplan,et al.  Regulation of iron acquisition and storage: consequences for iron-linked disorders , 2008, Nature Reviews Molecular Cell Biology.

[107]  J. Pieters,et al.  Mycobacterium tuberculosis and the macrophage: maintaining a balance. , 2008, Cell host & microbe.

[108]  O. Dussurget.  New insights into determinants of Listeria monocytogenes virulence. , 2008, International review of cell and molecular biology.

[109]  B. Finlay,et al.  Pathogenesis of enteric Salmonella infections , 2008, Current opinion in gastroenterology.

[110]  W. Eisenreich,et al.  Carbon metabolism of Listeria monocytogenes growing inside macrophages , 2008, Molecular microbiology.

[111]  E. Seto,et al.  Factors determining the heterogeneity of malaria incidence in children in Kampala, Uganda. , 2008, The Journal of infectious diseases.

[112]  Christopher M. Sassetti,et al.  Mycobacterial persistence requires the utilization of host cholesterol , 2008, Proceedings of the National Academy of Sciences.

[113]  M. Parker,et al.  During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems , 2008, Cellular microbiology.

[114]  Samuel I. Miller,et al.  Salmonellae interplay with host cells , 2008, Nature Reviews Microbiology.

[115]  W. Goebel,et al.  Glycerol Metabolism and PrfA Activity in Listeria monocytogenes , 2008, Journal of bacteriology.

[116]  D. Raoult,et al.  Regulation of whole bacterial pathogen transcription within infected hosts. , 2008, FEMS microbiology reviews.

[117]  P. Cossart,et al.  Conjugated action of two species-specific invasion proteins for fetoplacental listeriosis , 2008, Nature.

[118]  Xiao-Jiang Feng,et al.  Systems-level metabolic flux profiling identifies fatty acid synthesis as a target for antiviral therapy , 2008, Nature Biotechnology.

[119]  W. Goebel,et al.  Modulation of PrfA activity in Listeria monocytogenes upon growth in different culture media. , 2008, Microbiology.

[120]  J. Vogel,et al.  Noncoding RNA control of the making and breaking of sugars. , 2008, Genes & development.

[121]  D. Vitkup,et al.  New surveyor tools for charting microbial metabolic maps , 2008, Nature Reviews Microbiology.

[122]  Philip D. Butcher,et al.  Probing Host Pathogen Cross-Talk by Transcriptional Profiling of Both Mycobacterium tuberculosis and Infected Human Dendritic Cells and Macrophages , 2008, PloS one.

[123]  J. Lindon,et al.  Systems biology: Metabonomics , 2008, Nature.

[124]  F. García-del Portillo,et al.  Growth control in the Salmonella-containing vacuole. , 2008, Current opinion in microbiology.

[125]  P. Cossart,et al.  Listeria monocytogenes, a unique model in infection biology: an overview. , 2008, Microbes and infection.

[126]  M. Whiteley,et al.  Revisiting the host as a growth medium , 2008, Nature Reviews Microbiology.

[127]  M. Niederweis,et al.  Nutrient acquisition by mycobacteria. , 2008, Microbiology.

[128]  Sergio Grinstein,et al.  Antimicrobial mechanisms of phagocytes and bacterial evasion strategies , 2009, Nature Reviews Microbiology.

[129]  L. Cantley,et al.  Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation , 2009, Science.

[130]  B. Brüne,et al.  HIF-1 in the inflammatory microenvironment. , 2009, Experimental cell research.

[131]  Y. Fujita.  Carbon Catabolite Control of the Metabolic Network in Bacillus subtilis , 2009, Bioscience, biotechnology, and biochemistry.

[132]  K. Melican,et al.  Real-time live imaging to study bacterial infections in vivo. , 2009, Current opinion in microbiology.

[133]  C. Thompson,et al.  Differential expression of a virulence factor in pathogenic and non-pathogenic mycobacteria , 2009, Molecular microbiology.

[134]  T. Conway,et al.  Salmonella enterica Serovar Typhimurium Mutants Unable To Convert Malate to Pyruvate and Oxaloacetate Are Avirulent and Immunogenic in BALB/c Mice , 2009, Infection and Immunity.

[135]  Dirk Bumann,et al.  System-level analysis of Salmonella metabolism during infection. , 2009, Current opinion in microbiology.

[136]  R. Valdivia,et al.  Host-microbe interactions: bacteria. , 2009, Current opinion in microbiology.

[137]  S. Gottesman,et al.  The Crp-Activated Small Noncoding Regulatory RNA CyaR (RyeE) Links Nutritional Status to Group Behavior , 2008, Journal of bacteriology.

[138]  C. Dorman.  Global regulators and environmental adaptation in Gram-negative pathogens. , 2009, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[139]  L. Colosi,et al.  Generation of Branched-Chain Fatty Acids through Lipoate-Dependent Metabolism Facilitates Intracellular Growth of Listeria monocytogenes , 2009, Journal of bacteriology.

[140]  M. Collin,et al.  Bacterial Sensing and Signaling , 2009 .

[141]  E. McGhie,et al.  Salmonella takes control: effector-driven manipulation of the host , 2009, Current opinion in microbiology.

[142]  Kristina Schauer,et al.  Both Thiamine Uptake and Biosynthesis of Thiamine Precursors Are Required for Intracellular Replication of Listeria monocytogenes , 2009, Journal of bacteriology.

[143]  P. Sansonetti,et al.  Life on the inside: the intracellular lifestyle of cytosolic bacteria , 2009, Nature Reviews Microbiology.

[144]  A. Thompson,et al.  Glucose and Glycolysis Are Required for the Successful Infection of Macrophages and Mice by Salmonella enterica Serovar Typhimurium , 2009, Infection and Immunity.

[145]  S. Gordon,et al.  Mce3R, a TetR-type transcriptional repressor, controls the expression of a regulon involved in lipid metabolism in Mycobacterium tuberculosis. , 2009, Microbiology.

[146]  P. Cossart,et al.  Modeling human listeriosis in natural and genetically engineered animals , 2009, Nature Protocols.

[147]  C. Parsot.  Shigella type III secretion effectors: how, where, when, for what purposes? , 2009, Current opinion in microbiology.

[148]  M. Wagner.  Single-cell ecophysiology of microbes as revealed by Raman microspectroscopy or secondary ion mass spectrometry imaging. , 2009, Annual review of microbiology.

[149]  C. Dorman.  Nucleoid-associated proteins and bacterial physiology. , 2009, Advances in applied microbiology.

[150]  U. Sauer,et al.  13C-based metabolic flux analysis , 2009, Nature Protocols.

[151]  N. Freitag,et al.  Listeria monocytogenes — from saprophyte to intracellular pathogen , 2009, Nature Reviews Microbiology.

[152]  W. Goebel,et al.  The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-cell spread of Listeria , 2009, Nature Cell Biology.

[153]  W. Eisenreich,et al.  Carbon Metabolism of Enterobacterial Human Pathogens Growing in Epithelial Colorectal Adenocarcinoma (Caco-2) Cells , 2010, PloS one.

[154]  W. Eisenreich,et al.  Pyruvate Carboxylase Plays a Crucial Role in Carbon Metabolism of Extra- and Intracellularly Replicating Listeria monocytogenes , 2010, Journal of bacteriology.

[155]  W. Goebel,et al.  The major PEP-phosphotransferase systems (PTSs) for glucose, mannose and cellobiose of Listeria monocytogenes, and their significance for extra- and intracellular growth. , 2010, Microbiology.