Journal of Bioenergetics and Biomembranes

, Volume 25, Issue 6, pp 581–589 | Cite as

Transport across the bacterial outer membrane

  • Hiroshi Nikaido


Diffusion of small molecules across the outer membrane of gram-negative bacteria may occur through protein channels and through lipid bilayer domains. Among protein channels, many examples of trimeric porins, which produce water-filled diffusion channels, are known. Although the channels are nonspecific, the diffusion rates of solutes are often drastically affected by their gross physicochemical properties, such as size, charge, or lipophilicity, because the channel has a dimension not too different from that of the diffusing solutes. In the last few years, the structures of three such porins have been solved by X-ray crystallography. It is now known that a monomer unit traverses the membrane 16 times as β-strands, and one of the external loop folds back into the channel to produce a narrow constriction. Most of the static properties of the channel, such as the pore size and the position of the amino acids that produce the constriction, can now be explained by the three-dimensional structure. Controversy, however, still surrounds the issue of whether there are dynamic modulation of the channel properties in response to pH, ionic strength, or membrane potential, and of whether such responses are physiological. More recently, two examples of monomeric porins have been identified. These porins allow a very slow diffusion of solutes, but the reason for this low permeability is still unclear. Finally, channels with specific binding sites facilitate the diffusion of specific classes of nutrients, often those compounds that are too large to penetrate rapidly through the porin channels. Lipid bilayers in the outer membrane were shown to be perhaps 50- to 100-fold less permeable to uncharged, lipophilic molecules in comparison with the bilayers made of the usual glycerophospholipids. This is caused by the presence of a lipopolysaccharide leaflet in the bilayer, and more specifically, by the presence of a larger number of fatty acids in each lipid molecule, and by the absence of unsaturated fatty acids in the lipopolysaccharide structure.

Key words

Porin channel permeability membrane protein β-barrel lipopolysaccharide bilayer fluidity 


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  1. Bauer, K., Struyve, M., Bosch, D., Benz, R., and Tommassen, J. (1989).K. Biol. Chem. 264 16393–16398.Google Scholar
  2. Bellido, F., Martin, N. L., Siehnel, R. J., and Hancock, R. E. W. (1992).J. Bacteriol. 174 5196–5203.Google Scholar
  3. Benson, S. A., Occi, J. L. L., and Sampson, B. A. (1988).J. Mol. Biol. 203 961–970.Google Scholar
  4. Benz, R., Janko, K., and Lauger, P. (1979).Biochim. Biophys. Acta 551 238–247.Google Scholar
  5. Benz, R., Darveau, R. P., and Hancock, R. E. W. (1984).Eur. J. Biochem. 140 319–324.Google Scholar
  6. Benz. R., Schmidt, A., and Vos-Scheperkeuter, G. H. (1987).J. Membr. Biol. 100 21–29.Google Scholar
  7. Berrier, C., Coulombe, A., Houssin, C., and Ghazi, A. (1989).FEBS Lett. 259 27–32.Google Scholar
  8. Blachly-Dyson, E., Peng, S., Colombini, M., and Forte, M. (1990)Science 247 1233–1236.Google Scholar
  9. Bremer, E., Middendorf, J., Martinussen, J., and Valentin-Hansen, P. (1990).Gene 96 59–65.Google Scholar
  10. Buechner, M., Delcour, A. H., Martinac, B., Adler, J., and Kung, C. (1990).Biochim. Biophys. Acta 1024 111–121.Google Scholar
  11. Cowan, S. W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R. A., Jansonius, J. N., and Rosenbusch, J. P. (1992).Nature (London),358 727–733.Google Scholar
  12. Death, A., Notley, L., and Ferenci, T. (1993).J. Bacteriol. 175 1475–1483.Google Scholar
  13. Ferenci, T., and Lee, K.-S. (1982).J. Mol. Biol. 160 431–444.Google Scholar
  14. Ferenci, T., Saurin, W., and Hofnung, M. (1988).J. Mol. Biol. 201 493–496.Google Scholar
  15. Forst, D., Schulein, K., Wacker, T., Diedrichs, K., Kreutz, W., Benz, R., and Welte, W. (1993).J. Mol. Biol. 229 258–262.Google Scholar
  16. Freundlieb, S., Ehmann, U., and Boos, W. (1988).J. Biol. Chem. 263 314–320.Google Scholar
  17. Garavito, R. M., and Rosenbusch, J. P. (1980).J. Cell. Biol. 86 327–329.Google Scholar
  18. Hancock, R. E. W., and Benz, R. (1986).Biochim. Biophys. Acta 860 699–707.Google Scholar
  19. Hancock, R. E. W., and Carey, A. M. (1979).J. Bacteriol. 140 902–910.Google Scholar
  20. Hancock, R. E. W., Poole. K., and Benz, R. (1982).J. Bacteriol. 150 730–738.Google Scholar
  21. Hancock, R. E. W., Egli, C., Benz, R., and Siehnel, R. J. (1992).J. Bacteriol. 174 471–476.Google Scholar
  22. Heine, H.-G., Francis, G., Lee, K.-S., and Ferenci, T. (1988).J. Bacteriol. 170 1730–1738.Google Scholar
  23. Jap, B. K., and Walian, P. J. (1990).Q. Rev. Biophys. 23 367–403.Google Scholar
  24. Jap, B. K., Walian, P. J., and Gehring, K. (1991).Nature (London),350 167–170.Google Scholar
  25. Labischinski, H., Barnickel, G., Bradaczek, H., Naumann, D., Rietschel, E. T., and Giesbrecht, P. (1985).J. Bacteriol. 169 9–20.Google Scholar
  26. Labischinski, H., Naumann, D., Shulz, C., Kusumoto, S., Shiba, T., Rietschel, E. T., and Giesbrecht, P. (1989).Eur. J. Biochem. 179 659–665.Google Scholar
  27. Levy, S. B. (1992).Antimicrob. Agents Chemother. 36 695–703.Google Scholar
  28. Luckey, M., and Nikaido, H. (1980).Proc. Natl. Acad. Sci. USA 77 167–171.Google Scholar
  29. Maier, C., Bremer, E., Schmid, A., and Benz, R. (1988).J. Biol. Chem. 263 2493–2499.Google Scholar
  30. Martinac, B., Buechner, M., Delcour, A. H., Adler, J., and Kung, C. (1987).Proc. Natl. Acad. Sci. USA 84 2297–2301.Google Scholar
  31. Misra, R., and Benson, S. A. (1988).J. Bacteriol. 170 3611–3617.Google Scholar
  32. Nikaido, H. (1990). InMembrane Transport and Information Storage. Advances in Membrane Fluidity, Vol. 4 (Aloia, R. C., Curtain, C. C., and Gordon, L. M., eds.), Alan, R. Liss, New York, pp. 165–190.Google Scholar
  33. Nikaido, H. (1992).Mol. Microbiol. 6 435–442.Google Scholar
  34. Nikaido, H., and Vaara, M. (1985).Microbiol. Rev. 49 1–32.Google Scholar
  35. Nikaido, H., Takeuchi, Y., Ohnishi, S., and Nakae, T. (1977)Biochim. Biophys. Acta 465 152–164.Google Scholar
  36. Nikaido, H., Nikaido, K., and Harayama, S. (1991).J. Biol. Chem. 266 770–779.Google Scholar
  37. Nikaido, H., Kim, S.-H., and Rosenberg, E. Y. (1993).Mol. Microbiol. 8 1025–1030.Google Scholar
  38. Pauptit, R. A., Schirmer, T., Jansonius, J. N., Rosenbusch, J. P., Parker, M. W., Tucker, A. D., Tsernoglou, D., Weiss, M. S., and Schulz, G. E. (1991).J. Struct. Biol. 107 136–145.Google Scholar
  39. Plesiat, P., and Nikaido, H. (1992).Mol. Microbiol. 6 1323–1333.Google Scholar
  40. Quinn, J. P., Dudek, C. A., di Vicenzo, C. A., Lucks, D. A., and Lerner, S. A. (1986).J. Infect. Dis. 154 289–294.Google Scholar
  41. Rachel, R., Engel, A. M., Huber, R., Stetter, K.-O., and Baumeister, W. (1990).FEBS Lett. 262 64–68.Google Scholar
  42. Schiltz, E., Kreusch, A., Nestel, U., and Schulz, G. E. (1991).Eur. J. Biochem. 199 587–594.Google Scholar
  43. Schulein, K., Schmid, A., and Benz, R. (1991).Mol. Microbiol. 5 2233–2241.Google Scholar
  44. Sen, K., and Nikaido, H. (1990).Proc. Natl. Acad. Sci. USA 87 743–747.Google Scholar
  45. Sen, K., and Nikaido, H. (1991).J. Bacteriol. 173 926–928.Google Scholar
  46. Sen, K., Hellman, J., and Nikaido, H. (1988).J. Biol. Chem. 263 1182–1187.Google Scholar
  47. Stein, W. D. (1967).The Movement of Molecules across Cell Membranes. Academic Press, New York.Google Scholar
  48. Struyve, M., Visser, J., Adriaanse, H., Benz, R., and Tommassen, J. (1993).Mol. Microbiol. 7 131–140.Google Scholar
  49. Sugawara, E., and Nikaido, H. (1992).J. Biol. Chem. 267 2507–2511.Google Scholar
  50. Takeuchi, Y., and Nikaido, H. (1981).Biochemistry 20 523–529.Google Scholar
  51. Todt, J. C., Rocque, W. J., and McGroarty, E. J. (1992).Biochemistry 31 10471–10478.Google Scholar
  52. Trias, J., and Nikaido, H. (1990).J. Biol. Chem. 265 15680–15684.Google Scholar
  53. Trias, J., Rosenberg, E. Y., and Nikaido, H. (1988).Biochim. Biophys. Acta 938 493–496.Google Scholar
  54. Trias, J., Dufresne, J., Levesque, R. C., and Nikaido, H. (1989).Antimicrob. Agents Chemother. 33 1201–1206.Google Scholar
  55. Trias, J., Jarlier, V., and Benz, R. (1992).Science 258 1479–1481.Google Scholar
  56. Vaara, M. (1992).Microbiol. Rev. 56 395–411.Google Scholar
  57. Vaara, M. (1993).Antimicrob. Agents Chemother., in press.Google Scholar
  58. Weiss, M. S., and Schulz, G. E. (1992).J. Mol. Biol. 227 493–509.Google Scholar
  59. Weiss, M. S., Abele, U., Weckesser, J., Welte, W., Shiltz, E., and Schulz, G. E. (1991).Science 254 1627–1629.Google Scholar
  60. Yoshimoto, T., Higashi, H., Kanatani, A., Lin, X.-S., Nagai, H., Oyama, H., Kurazono, K., and Tsuru, D. (1991).J. Bacteriol. 173 2173–2179.Google Scholar
  61. Yoshimura, F., and Nikaido, H. (1982).J. Bacteriol. 152 636–642.Google Scholar
  62. Zimmermann, W., and Rosselet, A. (1977).Antimicrob. Agents Chemother. 12 368–372.Google Scholar
  63. Zoratti, M., and Petronilli, V. (1988).FEBS Lett. 240 105–109.Google Scholar

Copyright information

© Plenum Publishing Corporation 1993

Authors and Affiliations

  • Hiroshi Nikaido
    • 1
  1. 1.Department of Molecular and Cell Biology, 229 Stanley HallUniversity of CaliforniaBerkeley

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