1887

Abstract

SUMMARY

A facultatively oligotrophic ultramicrobacterium (strain RB2256) isolated from an Alaskan fjord by extinction dilution in seawater, was grown in batch culture and under single- and dual-substrate-limitation of alanine and glucose in a chemostat. The nature of the uptake systems, and the uptake kinetics and utilization patterns of alanine and glucose were investigated. Glucose uptake was inducible, the system exhibited a narrow substrate specificity, and part of the uptake system was osmotic-shock-sensitive. Half-saturation constants for glucose were between 7 and 74 μM during glucose limitation. The initial step in glucose metabolism was the synthesis of sugar polymers, even during glucose-limited growth. The alanine uptake system was constitutively expressed and was binding-protein-dependent. In addition to L-alanine, nine other amino acids inhibited accumulation of [C]L-alanine, indicating broad substrate specificity of the alanine transporter. Half-saturation constants between 1·3 and 1·8 μM were determined for alanine uptake during alanine limitation. Simultaneous utilization of glucose and alanine occurred during substrate-limited growth in the chemostat, and during growth in batch culture at relatively high (mM) substrate concentrations. However, the half-saturation constant for alanine transport during dual-substrate-limitation, i.e. in the presence of glucose, increased almost fivefold. We conclude that mixed substrate utilization is an inherent property of this organism.

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1995-02-01
2021-08-05
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References

  1. Abee T., van der Wal F.-J., Hellingwerf K. J., Konings W. N. 1989; Binding-protein-dependent alanine transport in Rhodobacter sphaerodes is regulated by the internal pH. J Bacterial 171:5148–5154
    [Google Scholar]
  2. Akagi Y., Taga N. 1980; Uptake of D-glucose and L-proline by oligotrophic and heterotrophic marine bacteria. Can J Microbiol 26:454–459
    [Google Scholar]
  3. Ammerman J. W., Fuhrman J. A., Hagström Å., Azam F. 1984; Bacterioplankton growth in seawater. I. Growth kinetics and cellular characteristics in seawater cultures. Mar Ecol Prog Ser 18:31–39
    [Google Scholar]
  4. Bakker E. P., Borchard A., Michels M., Altendorf K., Siebers M. 1987; High-affinity potassium uptake system in Bacillus acidocaldarius showing immunological cross-reactivity with the Kdp system from Escherichia coli. . J Bacterial 169:4342–4348
    [Google Scholar]
  5. Billen G., Joris C., Wijnant J., Gillain G. 1980; Concentration and microbiological utilization of small organic molecules in the Scheldt estuary, the Belgian coastal zone of the North Sea and the English Channel. Estuarine Coastal Mar Sci 11:279–294
    [Google Scholar]
  6. Button D. K. 1991; Biochemical basis for whole-cell uptake kinetics: specific affinity, oligotrophic capacity, and the meaning of the Michaelis constant. Appl Environ Microbiol 57:2033–2038
    [Google Scholar]
  7. Button D. K. 1993; Nutrient-limited microbial growth kinetics: overview and recent advances. Antonie Eeeuwenhoek 63:225–235
    [Google Scholar]
  8. Carlucci A. F., Williams P. M. 1978; Simulated in situ growth rates of pelagic marine bacteria. Naturwissenschaften 65:541–542
    [Google Scholar]
  9. Egli Th., Lindley N. D., Quayle J. R. 1983; Regulation of enzyme synthesis and variation of residual methanol concentration during carbon-limited growth of Kloeckera sp. 2201 on mixtures of methanol and glucose. j Gen Microbiol 129:1269–1281
    [Google Scholar]
  10. Egli Th., Bosshard C., Hamer G. 1986; Simultaneous utilization of methanol-glucose mixtures by Hansenula polymorpha in chemostat: influence of dilution rate and mixture composition on utilization pattern. Biotechnol Bioeng 28:1735–1741
    [Google Scholar]
  11. Eguchi M., Ishida Y. 1990; Oligotrophic properties of heterotrophic bacteria and in situ heterotrophic activity in pelagic seawaters. FEMS Microbiol Ecol 73:23–30
    [Google Scholar]
  12. Fein J. E., MacLeod R. A. 1975; Characterization of neutral amino acid transport in a marine pseudomonad. J Bacterial 124:1177–1190
    [Google Scholar]
  13. Ferber D. M., Ely B. 1982; Resistance to amino acid inhibition in Caulobacter crescentus. . Mol & Gen Genet 187:446–452
    [Google Scholar]
  14. Ferguson R. L., Buckley E. N., Palumbo A. V. 1984; Response of bacterioplankton to differential filtration and confinement. Appl Environ Microbiol 47:49–55
    [Google Scholar]
  15. Furlong C. E. 1987 Osmotic-shock-sensitive transport systems. In Escherichia coli and Salmonella typhimurium pp 768–796 Edited by Neidhardt F. C., Ingraham J. L., Brooks Low K., Magasanik B., Schaechter M., Umbarger H. E. Washington, DC: American Society for Microbiology.;
    [Google Scholar]
  16. Geesey G. G., Morita Y. R. 1979; Capture of arginine at low concentrations by a marine psychrophilic bacterium. Appl Environ Microbiol 38:1092–1097
    [Google Scholar]
  17. Gottschal J. C., Harder W., Prins R. A. 1992 Principles of enrichment, isolation, cultivation and preservation of bacteria. In The Prokaryotes pp 149–196 Edited by Balows A., Trüper H. G., Dworkin M., Harder W., Schleifer K.-H. New York: SpringerVerlag;
    [Google Scholar]
  18. Hagström Å., Ammerman J. W., Henrichs S., Azam F. 1984; Bacterioplankton growth in seawater. II. Organic matter utilization during steady-state growth in seawater cultures. Mar Ecol Prog Ser 18:41–48
    [Google Scholar]
  19. Hamilton R. D., Morgan K. M., Strickland J. D. H. 1966; The glucose uptake kinetics of some marine bacteria. Can J Microbiol 21:995–1003
    [Google Scholar]
  20. Harder W., Dijkhuizen L. 1982; Strategies of mixed substrate utilization in microorganisms. Philos Trans R Soc Eond B Biol Sci 297:459–480
    [Google Scholar]
  21. Harder W., Dijkhuizen L. 1983; Physiological responses to nutrient limitation. Annu Rev Microbiol 37:1–23
    [Google Scholar]
  22. Hobbie J. E., Crawford C. C. 1969; Respiration corrections for bacterial uptake of dissolved organic compounds in natural waters. Limnol Oceanogr 14:528–532
    [Google Scholar]
  23. Hobson A. C., Weatherwax R., Ames G.F.-L. 1984; ATP- binding sites in the membrane components of histidine permease, a periplasmic transport system. Proc Natl Acad Sci USA 81:7333–7337
    [Google Scholar]
  24. Jannasch H. W. 1967; Growth of marine bacteria in limiting concentrations of organic carbon in seawater. Eimnol Oceanogr 12:264–271
    [Google Scholar]
  25. Karl D. M. 1979; Measurement of microbial activity and growth in the ocean by rates of stable ribonucleic acid synthesis. Appl Environ Microbiol 38:850–860
    [Google Scholar]
  26. Konings W. N., Veldkamp H. 1983 Energy transduction and solute transport mechanisms in relation to environments occupied by microorganisms. In Microbes in their Natural Environments Society for General Microbiology Symposium 34 pp 153–186 Edited by Slater J. H., Whittenbury R., Wimpenny J. W. T. Cambridge: Cambridge University Press.;
    [Google Scholar]
  27. Law A. T., Button D. K. 1977; Multiple -carbon-source-limited growth kinetics of a marine coryneform bacterium. J Bacterial 129:115–123
    [Google Scholar]
  28. Li W. K. W., Dickie P. M. 1985; Growth of bacteria in seawater filtered through 0·2 μm Nuclepore membranes: implications for dilution experiments.. Mar Ecol Prog Ser 26:245–252
    [Google Scholar]
  29. Magasanik B., Neidhardt F. C. 1987; Regulation of carbon and nitrogen utilization. In Escherichia coli and Salmonella typhimurium pp 1318–1325 Edited by Neidhardt F. C., Ingraham J. L., Brooks Low K., Magasanik B., Schaechter M., Umbarger H. E. Washington, DC: American Society for Microbiology.;
    [Google Scholar]
  30. Morita R. Y. 1988; Bioavailability of energy and its relationship to growth and starvation survival in nature. Can J Microbiol 34:436–441
    [Google Scholar]
  31. Morita R. Y. 1990; The starvation-survival state of microorganisms in nature and its relationship to the bioavailable energy. Experientia 46:813–817
    [Google Scholar]
  32. Münster U. 1993; Concentrations and fluxes of organic carbon substrates in the aquatic environment. Antonie Eeeuwenhoek 63:243–274
    [Google Scholar]
  33. Nissen H., Nissen P., Azam F. 1984; Multiphasic uptake of D-glucose by an oligotrophic marine bacterium. Mar Ecol Prog Ser 16:155–160
    [Google Scholar]
  34. Poindexter J. S. 1981; Oligotrophy. Fast and famine existence. Adv Microb Ecol 5:63–89
    [Google Scholar]
  35. Poindexter J. S. 1987 Bacterial responses to nutrient limitation. In:Ecology of Microbial Communities Society for General Microbiology Symposium 41 pp 283–317 Edited by Fletcher M., Gray T. R. G., Jones J. G. Cambridge: Cambridge University Press.;
    [Google Scholar]
  36. Poulet S. A., Martin-Jézéquel V., Head R. N. 1984; Distribution of dissolved free amino acids in the Ushant front region. Mar Ecol Prog Ser 18:49–55
    [Google Scholar]
  37. Rahmanian M., Claus D. R., Oxender D. L. 1973; Multiplicity of leucine transport systems in Escherichia coli K-12. J Bacterial 116:1258–1266
    [Google Scholar]
  38. Richarme G., Kepes A. 1983; Study of binding protein-ligand interaction by ammonium sulphate-assisted adsorption on cellulose esters filters. Biochim Biophys Acta 742:16–24
    [Google Scholar]
  39. Robillard G. T., Blaauw M. 1987; Enzyme II of the Escherichia coli phosphoenolpyruvate dependent phosphotransferase system: protein-protein and protein-phospholipid interaction. Biochemistry 26:5796–5803
    [Google Scholar]
  40. Schut F., de Vries E. J., Gottschal J. C., Robertson B. R., Harder W., Prins R. A., Button D. K. 1993; Isolation of typical marine bacteria by dilution culture: growth, maintenance, and characteristics of isolates under laboratory conditions. Appl Environ Microbiol 59:2150–2160
    [Google Scholar]
  41. Sieburth J. McN, Johnson K. M., Burney C. M., Lavoie D. M. 1977; Estimation of in situ rates of heterotrophy using diurnal changes in dissolved organic matter and growth rates of picoplankton in diffusion culture. Helgol Wiss Meeresunters 30:565–574
    [Google Scholar]
  42. Upton A. C., Nedwell D. B. 1989; Nutritional flexibility of oligotrophic and copiotrophic Antarctic bacteria with respect to organic substrates. FEMS Microbiol Ecol 62:1–6
    [Google Scholar]
  43. Yabuuchi E., Yano I., Oyaizu H., Hashimoto Y., Ezaki T., Yamamoto H. 1990; Proposals of Sphingomonas paucimobilis gen. nov. and comb, nov., Sphingomonas parapaucimobilis sp. nov., Sphingomonas yanoikuyae sp. nov., Sphingomonas adhaesiva sp. nov., Sphingomonas capsulata comb, no v., and two genospecies of the genus Sphingomonas. . Microbiol Immunol 34:99–110
    [Google Scholar]
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