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How close to the theoretical diffusion limit do bacterial uptake systems function?

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Abstract

Using a 10cm flow-through cuvette in a high precision spectrophotometer linked to a mini-computer, the growth rate dependence of Escherichia coli on glucose concentration has been studied. The specific growth rate vs bacterial mass of single cultures consuming small amounts of glucose was followed. The data were analyzed with the computer programs described previously. For neither batch nor chemostat-cultured organisms did growth follow the monod growth law. Rather, the growth rate vs residual glucose concentration has an almost abrupt change in slope, indicative of a passive diffusion barrier prior to an uptake system possessing hyperbolic dependency. Calculations showed that the diffusion through the outer membrane via the porin channels could quantitatively account for the deviations from hyperbolic dependency. Long term chemostat culture alters the bacteria so that the maximum specific growth rate is reduced, but the initial dependence on glucose concentration is increased approaching more closely the theoretical limit. Therefore there was both a change in the outer membrane channels and the uptake activity of the cytoplasmic membrane.

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References

  • Ames GF (1964) Uptake of amino acids by Salmonella typhimurium. Arch Biochem Biophys 104:1–18

    Google Scholar 

  • Anderson RP, Roth JR (1977) Tandem genetic duplications in phage and bacteria. Ann Rev Microbiol 31:473–505

    Google Scholar 

  • Bavoil P, Nikaido H, von Meyenburg K (1977) Pleiotropic transport mutants of Escherichia coli lack porin, a major outer membrane protein. Molec Gen Genet 158:22–33

    Google Scholar 

  • DiRienzo JM, Nakamura K, Inouye M (1978) The outer membrane protein of gram-negative bacteria: biosynthesis, assembly, and function. Ann Rev Biochem 47:481–532

    Google Scholar 

  • Dykhuizen D (1978) Selection for tryphophan auxotrophs of Escherichia coli in glucose-limited chemostats as a test of the energy conservation hypothesis of evolution. Evolution 32:125–150

    Google Scholar 

  • Inouye M (1974) A three-dimensional molecular assembly model of a lipoprotein from Escherichia coli outer membrane. Proc Natl Acad Sci (Wash) 91:2396–2400

    Google Scholar 

  • Jannasch HW (1968) Competitive elimination of Enterobacteriaceae from seawater. Applied Microbiol 16:1616–1618

    Google Scholar 

  • Koch AL (1960) Encounter efficiency of coliphage-bacterium interaction. Biochim Biophys Acta 39:273–292

    Google Scholar 

  • Koch AL (1971) The adaptive response of Escherichia coli to a feast and famine existence. Adv Microbiol Physiol 6:147–217

    Google Scholar 

  • Koch AL (1979a) Selection and recombination in populations containing tandem multiplet genes. J Mol Evol 14:273

    Google Scholar 

  • Koch AL (1979b) Microbial growth in low concentrations of nutrients. In: S. Bernhard (ed) Life sciences research report, 13. M. Shilo (ed) Strategies of microbial life in extreme environments. Verlag Chemie, Weinheim, pp 261–279

    Google Scholar 

  • Koch AL (1982) Multistep kinetics: Choice of models for the growth of bacteria. J Theoret Biol (in press)

  • Koch AL, Coffman R (1970) Diffusion, permeation, or enzyme limitation: A probe for the kinetics of enzyme induction. Biotechnol Bioeng XII, 651–677

    Google Scholar 

  • Matin A, Veldkamp H (1978) Physiological basis of the selective advantage of a Spirillum sp. in a carbon-limited enviroment. J Gen Microbiol 105:187–197

    Google Scholar 

  • Monod J (1942) Recherches sur la croissance des cultures bactériennes. Hermann Cie, Paris

    Google Scholar 

  • Moser H (1958) The dynamics of bacterial populations. Carnegie Institution of Washington, Washington, pp 1–136

    Google Scholar 

  • Nakae T (1976) Outer membrane of Salmonella. Isolation of protein complex that produces transmembrane channels. J Biol Chem 251:2176–2178

    Google Scholar 

  • Nikaido H (1979) Nonspecific transport through the outer membrane. In: M Inouye (ed) Bacterial outer membrane. Wiley & Sons, New York, pp 361–407

    Google Scholar 

  • Nikaido H, Rosenberg EY (1981) Effect of solute size on the diffusion rates through the transmembrane pores of the outer membrane of Escherichia coli. J Gen Physiol 11:121–135

    Google Scholar 

  • Powell EO (1967) The growth rate of microorganisms as a function of substrate concentration. In: EO Powell, C Evans, RE Strange, and DW Tempest (eds) Microbial physiology and continuous culture. Her Majesty's Stationary Office, London, pp 34–55

    Google Scholar 

  • Renkin EM (1954) Filtration, diffusion, and molecular sieving through porous cellulose membranes. J Gen Physiol 38:225–243

    Google Scholar 

  • Riley M, Anilionis A (1978) Evolution of the bacterial genome. Ann Rev Microbiol 32:519–560

    Google Scholar 

  • Shehata TE, Marr AG (1971) Effect of nutrient concentration on the growth of Escherichia coli. J Bacteriol 107:210–216

    Google Scholar 

  • Steven AC, Ten Heggler B, Muller R, Kistler J, Rosenbusch JP (1971) Ultrastructure of a periodie protein layer in the outer membrane of Escherichia coli. J Cell Biol 72:292–301

    Google Scholar 

  • Stock JB, Rauch B, Roseman S (1977) Periplasmic space in Salmonella typhimurium and Escherichia coli. J Biol Chem 252:7850–7861

    Google Scholar 

  • Von Meyenburg K (1971) Transport-limited growth rates in a mutantant of Escherichia coli. J Bacteriol 107:878–888

    Google Scholar 

  • Wang CH, Koch AL (1978) Constancy of growth on simple and complex media. J Bacteriol 136:969–975

    Google Scholar 

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Koch, A.L., Houston Wang, C. How close to the theoretical diffusion limit do bacterial uptake systems function?. Arch. Microbiol. 131, 36–42 (1982). https://doi.org/10.1007/BF00451496

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  • DOI: https://doi.org/10.1007/BF00451496

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