1887

Abstract

The growth and nutritional requirements of mycobacteria have been intensively studied since the discovery of more than a century ago. However, the identity of many transporters for essential nutrients of and other mycobacteria is still unknown despite a wealth of genomic data and the availability of sophisticated genetic tools. Recently, considerable progress has been made in recognizing that two lipid permeability barriers have to be overcome in order for a nutrient molecule to reach the cytoplasm of mycobacteria. Uptake processes are discussed by comparing with . For example, has only five recognizable carbohydrate transporters in the inner membrane, while has 28 such transporters at its disposal. The specificities of inner-membrane transporters for sulfate, phosphate and some amino acids have been determined. Outer-membrane channel proteins in both organisms are thought to contribute to nutrient uptake. In particular, the Msp porins have been shown to be required for uptake of carbohydrates, amino acids and phosphate by . The set of porins also appears to be different for and . These differences likely reflect the lifestyles of these mycobacteria and the availability of nutrients in their natural habitats: the soil and the human body. The comprehensive identification and the biochemical and structural characterization of the nutrient transporters of will not only promote our understanding of the physiology of this important human pathogen, but might also be exploited to improve tuberculosis chemotherapy.

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2008-03-01
2019-11-21
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References

  1. Agranoff, D. & Krishna, S. ( 2004; ). Metal ion transport and regulation in Mycobacterium tuberculosis. Front Biosci 9, 2996–3006.[CrossRef]
    [Google Scholar]
  2. Barry, C. E., III, Lee, R. E., Mdluli, K., Sampson, A. E., Schroeder, B. G., Slayden, R. A. & Yuan, Y. ( 1998; ). Mycolic acids: structure, biosynthesis and physiological functions. Prog Lipid Res 37, 143–179.[CrossRef]
    [Google Scholar]
  3. Bell, A. W., Buckel, S. D., Groarke, J. M., Hope, J. N., Kingsley, D. H. & Hermodson, M. A. ( 1986; ). The nucleotide sequences of the rbsD, rbsA, and rbsC genes of Escherichia coli K12. J Biol Chem 261, 7652–7658.
    [Google Scholar]
  4. Bentley, S. D., Chater, K. F., Cerdeno-Tarraga, A. M., Challis, G. L., Thomson, N. R., James, K. D., Harris, D. E., Quail, M. A., Kieser, H. & other authors ( 2002; ). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417, 141–147.[CrossRef]
    [Google Scholar]
  5. Bertram, R., Schlicht, M., Mahr, K., Nothaft, H., Saier, M. H., Jr & Titgemeyer, F. ( 2004; ). In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J Bacteriol 186, 1362–1373.[CrossRef]
    [Google Scholar]
  6. Beveridge, T. J. ( 1995; ). The periplasmic space and the periplasm in Gram-positive and Gram-negative bacteria. ASM News 61, 125–130.
    [Google Scholar]
  7. Beveridge, T. J. ( 1999; ). Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181, 4725–4733.
    [Google Scholar]
  8. Beveridge, T. J. & Kadurugamuwa, J. L. ( 1996; ). Periplasm, periplasmic spaces, and their relation to bacterial wall structure: novel secretion of selected periplasmic proteins from Pseudomonas aeruginosa. Microb Drug Resist 2, 1–8.[CrossRef]
    [Google Scholar]
  9. Bhatt, K., Banerjee, S. K. & Chakraborti, P. K. ( 2000; ). Evidence that phosphate specific transporter is amplified in a fluoroquinolone resistant Mycobacterium smegmatis. Eur J Biochem 267, 4028–4032.[CrossRef]
    [Google Scholar]
  10. Borich, S. M., Murray, A. & Gormley, E. ( 2000; ). Genomic arrangement of a putative operon involved in maltose transport in the Mycobacterium tuberculosis complex and Mycobacterium leprae. Microbios 102, 7–15.
    [Google Scholar]
  11. Braibant, M., Lefevre, P., de Wit, L., Peirs, P., Ooms, J., Huygen, K., Andersen, A. B. & Content, J. ( 1996; ). A Mycobacterium tuberculosis gene cluster encoding proteins of a phosphate transporter homologous to the Escherichia coli Pst system. Gene 176, 171–176.[CrossRef]
    [Google Scholar]
  12. Braibant, M., Gilot, P. & Content, J. ( 2000; ). The ATP binding cassette (ABC) transport systems of Mycobacterium tuberculosis. FEMS Microbiol Rev 24, 449–467.[CrossRef]
    [Google Scholar]
  13. Braun, V. & Killmann, H. ( 1999; ). Bacterial solutions to the iron-supply problem. Trends Biochem Sci 24, 104–109.[CrossRef]
    [Google Scholar]
  14. Brennan, P. J. & Nikaido, H. ( 1995; ). The envelope of mycobacteria. Annu Rev Biochem 64, 29–63.[CrossRef]
    [Google Scholar]
  15. Brinkkötter, A., Kloss, H., Alpert, C. & Lengeler, J. W. ( 2000; ). Pathways for the utilization of N-acetylgalactosamine and galactosamine in Escherichia coli. Mol Microbiol 37, 125–135.[CrossRef]
    [Google Scholar]
  16. Chakrabarti, A. C. & Deamer, D. W. ( 1992; ). Permeability of lipid bilayers to amino acids and phosphate. Biochim Biophys Acta 1111, 171–177.[CrossRef]
    [Google Scholar]
  17. Chan, E. D., Chan, J. & Schluger, N. W. ( 2001; ). What is the role of nitric oxide in murine and human host defense against tuberculosis? Current knowledge. Am J Respir Cell Mol Biol 25, 606–612.[CrossRef]
    [Google Scholar]
  18. Clegg, S., Yu, F., Griffiths, L. & Cole, J. A. ( 2002; ). The roles of the polytopic membrane proteins NarK, NarU and NirC in Escherichia coli K-12: two nitrate and three nitrite transporters. Mol Microbiol 44, 143–155.[CrossRef]
    [Google Scholar]
  19. Cole, S. T., Brosch, R., Parkhill, J., Garnier, T., Churcher, C., Harris, D., Gordon, S. V., Eiglmeier, K., Gas, S. & other authors ( 1998; ). Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393, 537–544.[CrossRef]
    [Google Scholar]
  20. Content, J., Braibant, M., Connell, N. & Ainsa, J. A. ( 2005; ). Transport processes. In Tuberculosis and the Tubercle Bacillus, pp. 379–401. Edited by S. Cole, K. D. Eisenach, D. N. McMurray & W. R. Jacobs. Washington, DC: ASM Press.
  21. Cox, R. A. & Cook, G. M. ( 2007; ). Growth regulation in the mycobacterial cell. Curr Mol Med 7, 231–245.[CrossRef]
    [Google Scholar]
  22. Daffé, M. & Draper, P. ( 1998; ). The envelope layers of mycobacteria with reference to their pathogenicity. Adv Microb Physiol 39, 131–203.
    [Google Scholar]
  23. Daley, D. O., Rapp, M., Granseth, E., Melen, K., Drew, D. & von Heijne, G. ( 2005; ). Global topology analysis of the Escherichia coli inner membrane proteome. Science 308, 1321–1323.[CrossRef]
    [Google Scholar]
  24. Dirusso, C. C. & Black, P. N. ( 2004; ). Bacterial long chain fatty acid transport: gateway to a fatty acid-responsive signaling system. J Biol Chem 279, 49563–49566.[CrossRef]
    [Google Scholar]
  25. Draper, P. ( 1998; ). The outer parts of the mycobacterial envelope as permeability barriers. Front Biosci 3, D1253–D1261.
    [Google Scholar]
  26. Dubnau, E., Chan, J., Mohan, V. P. & Smith, I. ( 2005; ). Responses of Mycobacterium tuberculosis to growth in the mouse lung. Infect Immun 73, 3754–3757.[CrossRef]
    [Google Scholar]
  27. Dumas, F., Koebnik, R., Winterhalter, M. & van Gelder, P. ( 2000; ). Sugar transport through maltoporin of Escherichia coli. Role of polar tracks. J Biol Chem 275, 19747–19751.[CrossRef]
    [Google Scholar]
  28. Edson, N. L. ( 1951; ). The intermediary metabolism of the mycobacteria. Bacteriol Rev 15, 147–182.
    [Google Scholar]
  29. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M. & Hinton, J. C. ( 2003; ). Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47, 103–118.
    [Google Scholar]
  30. Etienne, G., Laval, F., Villeneuve, C., Dinadayala, P., Abouwarda, A., Zerbib, D., Galamba, A. & Daffe, M. ( 2005; ). The cell envelope structure and properties of Mycobacterium smegmatis mc2155: is there a clue for the unique transformability of the strain? Microbiology 151, 2075–2086.[CrossRef]
    [Google Scholar]
  31. Eze, M. O. & McElhaney, R. N. ( 1981; ). The effect of alterations in the fluidity and phase state of the membrane lipids on the passive permeation and facilitated diffusion of glycerol in Escherichia coli. J Gen Microbiol 124, 299–307.
    [Google Scholar]
  32. Faller, M., Niederweis, M. & Schulz, G. E. ( 2004; ). The structure of a mycobacterial outer-membrane channel. Science 303, 1189–1192.[CrossRef]
    [Google Scholar]
  33. Franke, W. & Schillinger, A. ( 1944; ). Zum Stoffwechsel der saeurefesten Bakterien. I. Orientierende aerobe Reihenversuche. Biochem Z 319, 313–334 (in German).
    [Google Scholar]
  34. Gebhard, S., Tran, S. L. & Cook, G. M. ( 2006; ). The Phn system of Mycobacterium smegmatis: a second high-affinity ABC-transporter for phosphate. Microbiology 152, 3453–3465.[CrossRef]
    [Google Scholar]
  35. Graham, L. L., Beveridge, T. J. & Nanninga, N. ( 1991; ). Periplasmic space and the concept of the periplasm. Trends Biochem Sci 16, 328–329.[CrossRef]
    [Google Scholar]
  36. Gutknecht, R., Beutler, R., Garcia-Alles, L. F., Baumann, U. & Erni, B. ( 2001; ). The dihydroxyacetone kinase of Escherichia coli utilizes a phosphoprotein instead of ATP as phosphoryl donor. EMBO J 20, 2480–2486.[CrossRef]
    [Google Scholar]
  37. Hancock, R. E., Farmer, S. W., Li, Z. S. & Poole, K. ( 1991; ). Interaction of aminoglycosides with the outer membranes and purified lipopolysaccharide and OmpF porin of Escherichia coli. Antimicrob Agents Chemother 35, 1309–1314.[CrossRef]
    [Google Scholar]
  38. Hoffmann, C., Leis, L., Niederweis, M., Plitzko, J. M. & Engelhardt, H. ( 2008; ). Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci U S A (in press).
    [Google Scholar]
  39. Izumori, K., Yamanaka, K. & Elbein, D. ( 1976; ). Pentose metabolism in Mycobacterium smegmatis: specificity of induction of pentose isomerases. J Bacteriol 128, 587–591.
    [Google Scholar]
  40. Jackson, M., Stadthagen, G. & Gicquel, B. ( 2007; ). Long-chain multiple methyl-branched fatty acid-containing lipids of Mycobacterium tuberculosis: biosynthesis, transport, regulation and biological activities. Tuberculosis 87, 78–86.[CrossRef]
    [Google Scholar]
  41. Jarlier, V. & Nikaido, H. ( 1990; ). Permeability barrier to hydrophilic solutes in Mycobacterium chelonei. J Bacteriol 172, 1418–1423.
    [Google Scholar]
  42. Jia, W. & Cole, J. A. ( 2005; ). Nitrate and nitrite transport in Escherichia coli. Biochem Soc Trans 33, 159–161.[CrossRef]
    [Google Scholar]
  43. Kana, B. D. & Mizrahi, V. ( 2004; ). Molecular genetics of Mycobacterium tuberculosis in relation to the discovery of novel drugs and vaccines. Tuberculosis 84, 63–75.[CrossRef]
    [Google Scholar]
  44. Kartmann, B., Stenger, S. & Niederweis, M. ( 1999; ). Porins in the cell wall of Mycobacterium tuberculosis. J Bacteriol 181, 6543–6546. (Authors' correction in J Bacteriol 181, 7650).
    [Google Scholar]
  45. Koch, R. ( 1882; ). Die Aetiologie der Tuberculose. Berliner Klinische Wochenzeitschrift 19, 18 (in German).
    [Google Scholar]
  46. Koebnik, R., Locher, K. P. & van Gelder, P. ( 2000; ). Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol Microbiol 37, 239–253.[CrossRef]
    [Google Scholar]
  47. Lichtinger, T., Heym, B., Maier, E., Eichner, H., Cole, S. T. & Benz, R. ( 1999; ). Evidence for a small anion-selective channel in the cell wall of Mycobacterium bovis BCG besides a wide cation-selective pore. FEBS Lett 454, 349–355.[CrossRef]
    [Google Scholar]
  48. Liu, J., Rosenberg, E. Y. & Nikaido, H. ( 1995; ). Fluidity of the lipid domain of cell wall from Mycobacterium chelonae. Proc Natl Acad Sci U S A 92, 11254–11258.[CrossRef]
    [Google Scholar]
  49. Liu, J., Barry, C. E., III, Besra, G. S. & Nikaido, H. ( 1996; ). Mycolic acid structure determines the fluidity of the mycobacterial cell wall. J Biol Chem 271, 29545–29551.[CrossRef]
    [Google Scholar]
  50. Machowski, E. E., Dawes, S. & Mizrahi, V. ( 2005; ). TB tools to tell the tale – molecular genetic methods for mycobacterial research. Int J Biochem Cell Biol 37, 54–68.[CrossRef]
    [Google Scholar]
  51. Mahfoud, M., Sukumaran, S., Hülsmann, P., Grieger, K. & Niederweis, M. ( 2006; ). Topology of the porin MspA in the outer membrane of Mycobacterium smegmatis. J Biol Chem 281, 5908–5915.
    [Google Scholar]
  52. Maier, C., Bremer, E., Schmid, A. & Benz, R. ( 1988; ). Pore-forming activity of the Tsx protein from the outer membrane of Escherichia coli. Demonstration of a nucleoside-specific binding site. J Biol Chem 263, 2493–2499.
    [Google Scholar]
  53. Matias, V. R. & Beveridge, T. J. ( 2005; ). Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol Microbiol 56, 240–251.[CrossRef]
    [Google Scholar]
  54. Matias, V. R. & Beveridge, T. J. ( 2006; ). Native cell wall organization shown by cryo-electron microscopy confirms the existence of a periplasmic space in Staphylococcus aureus. J Bacteriol 188, 1011–1021.[CrossRef]
    [Google Scholar]
  55. Matias, V. R., Al-Amoudi, A., Dubochet, J. & Beveridge, T. J. ( 2003; ). Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa. J Bacteriol 185, 6112–6118.[CrossRef]
    [Google Scholar]
  56. McAdam, R. A., Weisbrod, T. R., Martin, J., Scuderi, J. D., Brown, A. M., Cirillo, J. D., Bloom, B. R. & Jacobs, W. R., Jr ( 1995; ). In vivo growth characteristics of leucine and methionine auxotrophic mutants of Mycobacterium bovis BCG generated by transposon mutagenesis. Infect Immun 63, 1004–1012.
    [Google Scholar]
  57. McKinney, J. D., Honer zu Bentrup, K., Munoz-Elias, E. J., Miczak, A., Chen, B., Chan, W. T., Swenson, D., Sacchettini, J. C., Jacobs, W. R., Jr & Russell, D. G. ( 2000; ). Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406, 735–738.[CrossRef]
    [Google Scholar]
  58. Mills, C. D. ( 2001; ). Macrophage arginine metabolism to ornithine/urea or nitric oxide/citrulline: a life or death issue. Crit Rev Immunol 21, 399–425.
    [Google Scholar]
  59. Mineda, T., Ohara, N., Yukitake, H. & Yamada, T. ( 1998; ). The ribosomes contents of mycobacteria. New Microbiol 21, 1–7.
    [Google Scholar]
  60. Minnikin, D. E. ( 1982; ). Lipids: complex lipids, their chemistry, biosynthesis and roles. In The Biology of the Mycobacteria: Physiology, Identification and Classification, pp. 95–184. Edited by C. Ratledge & J. Stanford. London: Academic Press.
  61. Moir, J. W. & Wood, N. J. ( 2001; ). Nitrate and nitrite transport in bacteria. Cell Mol Life Sci 58, 215–224.[CrossRef]
    [Google Scholar]
  62. Molle, V., Saint, N., Campagna, S., Kremer, L., Lea, E., Draper, P. & Molle, G. ( 2006; ). pH-dependent pore-forming activity of OmpATb from Mycobacterium tuberculosis and characterization of the channel by peptidic dissection. Mol Microbiol 61, 826–837.[CrossRef]
    [Google Scholar]
  63. Munoz-Elias, E. J. & McKinney, J. D. ( 2005; ). Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat Med 11, 638–644.[CrossRef]
    [Google Scholar]
  64. Murphy, H. N., Stewart, G. R., Mischenko, V. V., Apt, A. S., Harris, R., McAlister, M. S., Driscoll, P. C., Young, D. B. & Robertson, B. D. ( 2005; ). The OtsAB pathway is essential for trehalose biosynthesis in Mycobacterium tuberculosis. J Biol Chem 280, 14524–14529.[CrossRef]
    [Google Scholar]
  65. Nathan, C. & Shiloh, M. U. ( 2000; ). Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97, 8841–8848.[CrossRef]
    [Google Scholar]
  66. Neyrolles, O., Hernandez-Pando, R., Pietri-Rouxel, F., Pietri-Rouxel, F., Fornès, P., Tailleux, L., Barrios Payán, J. A., Pivert, E., Bordat, Y., Aguilar, D. & other authors ( 2006; ). Is adipose tissue a place for Mycobacterium tuberculosis persistence? PLoS ONE 1, e43 [CrossRef]
    [Google Scholar]
  67. Niederweis, M. ( 2003; ). Mycobacterial porins – new channel proteins in unique outer membranes. Mol Microbiol 49, 1167–1177.[CrossRef]
    [Google Scholar]
  68. Niederweis, M., Ehrt, S., Heinz, C., Klöcker, U., Karosi, S., Swiderek, K. M., Riley, L. W. & Benz, R. ( 1999; ). Cloning of the mspA gene encoding a porin from Mycobacterium smegmatis. Mol Microbiol 33, 933–945.[CrossRef]
    [Google Scholar]
  69. Nikaido, H. ( 1994; ). Porins and specific diffusion channels in bacterial outer membranes. J Biol Chem 269, 3905–3908.
    [Google Scholar]
  70. Nikaido, H. ( 2003; ). Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67, 593–656.[CrossRef]
    [Google Scholar]
  71. Nikaido, H., Rosenberg, E. Y. & Foulds, J. ( 1983; ). Porin channels in Escherichia coli: studies with beta-lactams in intact cells. J Bacteriol 153, 232–240.
    [Google Scholar]
  72. Nikaido, H., Kim, S. H. & Rosenberg, E. Y. ( 1993; ). Physical organization of lipids in the cell wall of Mycobacterium chelonae. Mol Microbiol 8, 1025–1030.[CrossRef]
    [Google Scholar]
  73. Nolden, L., Ngouoto-Nkili, C. E., Bendt, A. K., Kramer, R. & Burkovski, A. ( 2001; ). Sensing nitrogen limitation in Corynebacterium glutamicum: the role of glnK and glnD. Mol Microbiol 42, 1281–1295.
    [Google Scholar]
  74. Nothaft, H., Dresel, D., Willimek, A., Mahr, K., Niederweis, M. & Titgemeyer, F. ( 2003; ). The phosphotransferase system of Streptomyces coelicolor is biased for N-acetylglucosamine metabolism. J Bacteriol 185, 7019–7023.[CrossRef]
    [Google Scholar]
  75. Ohno, H., Zhu, G., Mohan, V. P., Chu, D., Kohno, S., Jacobs, W. R., Jr & Chan, J. ( 2003; ). The effects of reactive nitrogen intermediates on gene expression in Mycobacterium tuberculosis. Cell Microbiol 5, 637–648.[CrossRef]
    [Google Scholar]
  76. Paul, T. R. & Beveridge, T. J. ( 1992; ). Reevaluation of envelope profiles and cytoplasmic ultrastructure of mycobacteria processed by conventional embedding and freeze-substitution protocols. J Bacteriol 174, 6508–6517.
    [Google Scholar]
  77. Paul, T. R. & Beveridge, T. J. ( 1994; ). Preservation of surface lipids and determination of ultrastructure of Mycobacterium kansasii by freeze-substitution. Infect Immun 62, 1542–1550.
    [Google Scholar]
  78. Paula, S., Volkov, A. G., Van Hoek, A. N., Haines, T. H. & Deamer, D. W. ( 1996; ). Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophys J 70, 339–348.[CrossRef]
    [Google Scholar]
  79. Peirs, P., Lefevre, P., Boarbi, S., Wang, X. M., Denis, O., Braibant, M., Pethe, K., Locht, C., Huygen, K. & Content, J. ( 2005; ). Mycobacterium tuberculosis with disruption in genes encoding the phosphate binding proteins PstS1 and PstS2 is deficient in phosphate uptake and demonstrates reduced in vivo virulence. Infect Immun 73, 1898–1902.[CrossRef]
    [Google Scholar]
  80. Ramakrishnan, T., Murthy, P. S. & Gopinathan, K. P. ( 1972; ). Intermediary metabolism of mycobacteria. Bacteriol Rev 36, 65–108.
    [Google Scholar]
  81. Ratledge, C. ( 1982; ). Nutrition, growth and metabolism. In The Biology of the Mycobacteria, pp. 186–212. Edited by C. Ratledge & J. Stanford. London: Academic Press.
  82. Ratledge, C. & Dover, L. G. ( 2000; ). Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54, 881–941.[CrossRef]
    [Google Scholar]
  83. Raynaud, C., Guilhot, C., Rauzier, J., Bordat, Y., Pelicic, V., Manganelli, R., Smith, I., Gicquel, B. & Jackson, M. ( 2002a; ). Phospholipases C are involved in the virulence of Mycobacterium tuberculosis. Mol Microbiol 45, 203–217.[CrossRef]
    [Google Scholar]
  84. Raynaud, C., Papavinasasundaram, K. G., Speight, R. A., Springer, B., Sander, P., Böttger, E. C., Colston, M. J. & Draper, P. ( 2002b; ). The functions of OmpATb, a pore-forming protein of Mycobacterium tuberculosis. Mol Microbiol 46, 191–201.[CrossRef]
    [Google Scholar]
  85. Rengarajan, J., Bloom, B. R. & Rubin, E. J. ( 2005; ). Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci U S A 102, 8327–8332.[CrossRef]
    [Google Scholar]
  86. Rimmele, M. & Boos, W. ( 1994; ). Trehalose-6-phosphate hydrolase of Escherichia coli. J Bacteriol 176, 5654–5664.
    [Google Scholar]
  87. Rodriguez, G. M. ( 2006; ). Control of iron metabolism in Mycobacterium tuberculosis. Trends Microbiol 14, 320–327.[CrossRef]
    [Google Scholar]
  88. Rodriguez, G. M. & Smith, I. ( 2006; ). Identification of an ABC transporter required for iron acquisition and virulence in Mycobacterium tuberculosis. J Bacteriol 188, 424–430.[CrossRef]
    [Google Scholar]
  89. Rowe, J. J., Ubbink-Kok, T., Molenaar, D., Konings, W. N. & Driessen, A. J. ( 1994; ). NarK is a nitrite-extrusion system involved in anaerobic nitrate respiration by Escherichia coli. Mol Microbiol 12, 579–586.[CrossRef]
    [Google Scholar]
  90. Russell, D. G. ( 2003; ). Phagosomes, fatty acids and tuberculosis. Nat Cell Biol 5, 776–778.[CrossRef]
    [Google Scholar]
  91. Sa-Nogueira, I., Nogueira, T. V., Soares, S. & de Lencastre, H. ( 1997; ). The Bacillus subtilis l-arabinose (ara) operon: nucleotide sequence, genetic organization and expression. Microbiology 143, 957–969.[CrossRef]
    [Google Scholar]
  92. Sassetti, C. M. & Rubin, E. J. ( 2003; ). Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100, 12989–12994.[CrossRef]
    [Google Scholar]
  93. Schnappinger, D., Ehrt, S., Voskuil, M. I., Liu, Y., Mangan, J. A., Monahan, I. M., Dolganov, G., Efron, B., Butcher, P. D. & other authors ( 2003; ). Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198, 693–704.[CrossRef]
    [Google Scholar]
  94. Schönert, S., Buder, T. & Dahl, M. K. ( 1999; ). Properties of maltose-inducible alpha-glucosidase MalL (sucrase-isomaltase-maltase) in Bacillus subtilis: evidence for its contribution to maltodextrin utilization. Res Microbiol 150, 167–177.[CrossRef]
    [Google Scholar]
  95. Senaratne, R. H., Mobasheri, H., Papavinasasundaram, K. G., Jenner, P., Lea, E. J. & Draper, P. ( 1998; ). Expression of a gene for a porin-like protein of the OmpA family from Mycobacterium tuberculosis H37Rv. J Bacteriol 180, 3541–3547.
    [Google Scholar]
  96. Seth, A. & Connell, N. D. ( 2000; ). Amino acid transport and metabolism in mycobacteria: cloning, interruption, and characterization of an l-Arginine/gamma-aminobutyric acid permease in Mycobacterium bovis BCG. J Bacteriol 182, 919–927.[CrossRef]
    [Google Scholar]
  97. Sohaskey, C. D. ( 2005; ). Regulation of nitrate reductase activity in Mycobacterium tuberculosis by oxygen and nitric oxide. Microbiology 151, 3803–3810.[CrossRef]
    [Google Scholar]
  98. Sohaskey, C. D. & Wayne, L. G. ( 2003; ). Role of narK2X and narGHJI in hypoxic upregulation of nitrate reduction by Mycobacterium tuberculosis. J Bacteriol 185, 7247–7256.[CrossRef]
    [Google Scholar]
  99. Sørensen, K. I. & Hove-Jensen, B. ( 1996; ). Ribose catabolism of Escherichia coli: characterization of the rpiB gene encoding ribose phosphate isomerase B and of the rpiR gene, which is involved in regulation of rpiB expression. J Bacteriol 178, 1003–1011.
    [Google Scholar]
  100. Stahl, C., Kubetzko, S., Kaps, I., Seeber, S., Engelhardt, H. & Niederweis, M. ( 2001; ). MspA provides the main hydrophilic pathway through the cell wall of Mycobacterium smegmatis. . Mol Microbiol 40, 451–464. (Authors' correction in Mol Microbiol 457, 1509).[CrossRef]
    [Google Scholar]
  101. Stephan, J., Bender, J., Wolschendorf, F., Hoffmann, C., Roth, E., Mailänder, C., Engelhardt, H. & Niederweis, M. ( 2005; ). The growth rate of Mycobacterium smegmatis depends on sufficient porin-mediated influx of nutrients. Mol Microbiol 58, 714–730.[CrossRef]
    [Google Scholar]
  102. Sumiya, M., Davis, E. O., Packman, L. C., McDonald, T. P. & Henderson, P. J. ( 1995; ). Molecular genetics of a receptor protein for d-xylose, encoded by the gene xylF, in Escherichia coli. Receptors Channels 3, 117–128.
    [Google Scholar]
  103. Talaue, M. T., Venketaraman, V., Hazbon, M. H., Peteroy-Kelly, M., Seth, A., Colangeli, R., Alland, D. & Connell, N. D. ( 2006; ). Arginine homeostasis in J774.1 macrophages in the context of Mycobacterium bovis BCG infection. J Bacteriol 188, 4830–4840.[CrossRef]
    [Google Scholar]
  104. Timm, J., Post, F. A., Bekker, L. G., Walther, G. B., Wainwright, H. C., Manganelli, R., Chan, W. T., Tsenova, L., Gold, B. & other authors ( 2003; ). Differential expression of iron-, carbon-, and oxygen-responsive mycobacterial genes in the lungs of chronically infected mice and tuberculosis patients. Proc Natl Acad Sci U S A 100, 14321–14326.[CrossRef]
    [Google Scholar]
  105. Titgemeyer, F., Amon, J., Parche, S., Mahfoud, M., Bail, J., Schlicht, M., Rehm, N., Hillmann, D., Stephan, J. & other authors ( 2007; ). A genomic view of sugar transport in Mycobacterium smegmatis and Mycobacterium tuberculosis. J Bacteriol 189, 5903–5915.[CrossRef]
    [Google Scholar]
  106. Trivedi, O. A., Arora, P., Sridharan, V., Tickoo, R., Mohanty, D. & Gokhale, R. S. ( 2004; ). Enzymic activation and transfer of fatty acids as acyl-adenylates in mycobacteria. Nature 428, 441–445.[CrossRef]
    [Google Scholar]
  107. Ulrichs, T. & Kaufmann, S. H. ( 2006; ). New insights into the function of granulomas in human tuberculosis. J Pathol 208, 261–269.[CrossRef]
    [Google Scholar]
  108. van Veen, H. W. ( 1997; ). Phosphate transport in prokaryotes: molecules, mediators and mechanisms. Antonie Van Leeuwenhoek 72, 299–315.[CrossRef]
    [Google Scholar]
  109. van Wezel, G. P., Mahr, K., Konig, M., Traag, B. A., Pimentel-Schmitt, E. F., Willimek, A. & Titgemeyer, F. ( 2005; ). GlcP constitutes the major glucose uptake system of Streptomyces coelicolor A3(2). Mol Microbiol 55, 624–636.
    [Google Scholar]
  110. Voskuil, M. I., Schnappinger, D., Visconti, K. C., Harrell, M. I., Dolganov, G. M., Sherman, D. R. & Schoolnik, G. K. ( 2003; ). Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198, 705–713.[CrossRef]
    [Google Scholar]
  111. Vyas, N. K., Vyas, M. N. & Quiocho, F. A. ( 2003; ). Crystal structure of M. tuberculosis ABC phosphate transport receptor: specificity and charge compensation dominated by ion-dipole interactions. Structure 11, 765–774.[CrossRef]
    [Google Scholar]
  112. Webb, M. R. ( 2003; ). Mycobacterial ABC transport system: structure of the primary phosphate receptor. Structure 11, 736–738.[CrossRef]
    [Google Scholar]
  113. Wheeler, P. R., Bulmer, K. & Ratledge, C. ( 1990; ). Enzymes for biosynthesis de novo and elongation of fatty acids in mycobacteria grown in host cells: is Mycobacterium leprae competent in fatty acid biosynthesis? J Gen Microbiol 136, 211–217.[CrossRef]
    [Google Scholar]
  114. Wolschendorf, F., Mahfoud, M. & Niederweis, M. ( 2007; ). Porins are required for uptake of phosphates by Mycobacterium smegmatis. J Bacteriol 189, 2435–2442.[CrossRef]
    [Google Scholar]
  115. Wood, K. V. ( 1995; ). Marker proteins for gene expression. Curr Opin Biotechnol 6, 50–58.[CrossRef]
    [Google Scholar]
  116. Woodruff, P. J., Carlson, B. L., Siridechadilok, B., Pratt, M. R., Senaratne, R. H., Mougous, J. D., Riley, L. W., Williams, S. J. & Bertozzi, C. R. ( 2004; ). Trehalose is required for growth of Mycobacterium smegmatis. J Biol Chem 279, 28835–28843.[CrossRef]
    [Google Scholar]
  117. Woodson, K. & Devine, K. M. ( 1994; ). Analysis of a ribose transport operon from Bacillus subtilis. Microbiology 140, 1829–1838.[CrossRef]
    [Google Scholar]
  118. Wooff, E., Michell, S. L., Gordon, S. V., Chambers, M. A., Bardarov, S., Jacobs, W. R., Jr, Hewinson, R. G. & Wheeler, P. R. ( 2002; ). Functional genomics reveals the sole sulphate transporter of the Mycobacterium tuberculosis complex and its relevance to the acquisition of sulphur in vivo. Mol Microbiol 43, 653–663.[CrossRef]
    [Google Scholar]
  119. Yabu, K. ( 1967; ). The uptake of d-glutamic acid by Mycobacterium avium. Biochim Biophys Acta 135, 181–183.[CrossRef]
    [Google Scholar]
  120. Yabu, K. ( 1970; ). Amino acid transport in Mycobacterium smegmatis. J Bacteriol 102, 6–13.
    [Google Scholar]
  121. Yabu, K. ( 1971; ). Aspartic acid transport in Mycobacterium smegmatis. Jpn J Microbiol 15, 449–456.[CrossRef]
    [Google Scholar]
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Genetic organization of carbohydrate transporters of the ABC family. The arrows indicate the length and transcriptional orientation of annotated genes and predicted open reading frames. Genes encoding transport systems are depicted in blue, carbohydrate metabolic genes are coloured in grey, regulatory genes are highlighted in red, while other genes are white. Genes are denominated by their number with the prefix 'msmeg_'. The gene names are assigned according to the annotations given by The Institute for Genomic Research ( http://www.tigr.org) and by Titgemeyer (2007). Numbers in parentheses refer to the intergenic distance between two genes. General gene designations are: , unknown reading frame; , sugar dehydrogenase; , sugar kinase; , sugar permease; , unspecified substrate binding protein of an ABC permease; and , denote unspecified membrane proteins of an ABC permease. [ PDF] (296 kb) Genetic organizition of carbohydrate transporters of the PTS, MIP, SSS and MFS protein families. For explanations see legend to Fig. S1. [ PDF] (125 kb) A genomic view of sugar transport in and . , 5903-5915.

PDF

Genetic organization of carbohydrate transporters of the ABC family. The arrows indicate the length and transcriptional orientation of annotated genes and predicted open reading frames. Genes encoding transport systems are depicted in blue, carbohydrate metabolic genes are coloured in grey, regulatory genes are highlighted in red, while other genes are white. Genes are denominated by their number with the prefix 'msmeg_'. The gene names are assigned according to the annotations given by The Institute for Genomic Research ( http://www.tigr.org) and by Titgemeyer (2007). Numbers in parentheses refer to the intergenic distance between two genes. General gene designations are: , unknown reading frame; , sugar dehydrogenase; , sugar kinase; , sugar permease; , unspecified substrate binding protein of an ABC permease; and , denote unspecified membrane proteins of an ABC permease. [ PDF] (296 kb) Genetic organizition of carbohydrate transporters of the PTS, MIP, SSS and MFS protein families. For explanations see legend to Fig. S1. [ PDF] (125 kb) A genomic view of sugar transport in and . , 5903-5915.

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