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Glycine betaine and proline are the principal compatible solutes ofStaphylococcus aureus

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Abstract

The foodborne pathogenStaphylococcus aureus is distinguished by its ability to grow within environments of extremely high osmolarity (e.g., foods with low water activity values). In the present study, we examined the accumulation of intracellular organic solutes withinS. aureus strain ATCC 12600 when cells were grown in a complex medium containing high concentrations of NaCl. Consistent with previous reports [Measures JC (1975) Nature 257:398–400; Koujima I, et al. (1978) Appl Environ Microbiol 35:467–470; and Anderson CB, Witter LD (1982) Appl Environ Microbiol 43:1501–1503], intracellular proline was found to accumulate to high concentrations. However, NMR spectroscopy of cell extracts revealed glycine betaine to be the predominant intracellular organic solute accumulated within cells grown at high osmolarity. In additional experiments, we examined the growth rate ofS. aureus in a defined medium of high osmolarity and found it to be stimulated significantly by the presence of either exogenous proline or glycine betaine. Highest growth rates were obtained when the defined medium was supplemented with glycine betaine.

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Literature Cited

  1. Abe I, Tsujioka H, Wasa T (1988) Solvent extraction cleanup for pre-treatment in amino acid analysis by gas chromatography. J Chromatog 449:165–174

    Google Scholar 

  2. Anderson CB, Witter LD (1982) Glutamine and proline accumulation byStaphylococcus aureus with reduction in water activity. Appl Environ Microbiol 43:1501–1503

    PubMed  Google Scholar 

  3. Bae J-H, Miller KJ (1990) Characterization of two proline transport systems inStaphylococcus aureus and their possible roles in osmotic adaptation. Abstracts of the Annual Meeting of the American Society for Microbiology 1990:283

  4. Banwart GJ (1981) Basic food microbiology. New York: Van Nostrand Reinhold

    Google Scholar 

  5. Bergdoll MS (1989)Staphylococcus aureus. In: Doyle MP, (ed) Foodborne bacterial pathogens. New York: Marcel Dekker, pp 463–523

    Google Scholar 

  6. Booth IR, Cairney J, Sutherland L, Higgins CF (1988) Enteric bacteria and osmotic stress: an integrated homeostatic system. J Appl Bacteriol Symp Suppl Series No. 17, pp 35S–49S

  7. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    PubMed  Google Scholar 

  8. Brown AD, Simpson JR (1972) Water relations of sugar-tolerant yeasts: the role of intracellular polyols. J Gen Microbiol 72:589–591

    PubMed  Google Scholar 

  9. Christian JHB, Waltho JA (1961) The sodium and potassium content of non-halophilic bacteria in relation to salt tolerance. J Gen Microbiol 25:97–102

    PubMed  Google Scholar 

  10. Christian JHB, Waltho JA (1962) Solute concentrations within cells of halophilic and non-halophilic bacteria. Biochim Biophys Acta 65:506–508

    PubMed  Google Scholar 

  11. Christian JHB, Waltho JA (1964) The composition ofStaphylococcus aureus in relation to the water activity of the growth medium. J Gen Microbiol 35:205–218

    PubMed  Google Scholar 

  12. Csonka LN (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53:121–147

    PubMed  Google Scholar 

  13. Genigeorgis CA (1989) Present state of knowledge on staphylococcal intoxication. Int J Food Microbiol 9:327–360

    PubMed  Google Scholar 

  14. Grothe S, Krogsrud RL, McClellan DJ, Milner JL, Wood JM (1986) Proline transport and osmotic stress response inEscherichia coli K-12. J Bacteriol 166:253–259

    PubMed  Google Scholar 

  15. Hanson RS, Philiips JA (1981) Chemical composition. In: Gerhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, Krieg NR, Phillips GB (eds) Manual of methods for general bacteriology. Washington, DC: American Society for Microbiology, pp 328–364

    Google Scholar 

  16. Hocking AD (1988) Strategies for microbial growth at reduced water activities. Microbiol Sci 5:280–284

    PubMed  Google Scholar 

  17. Hutkins RW, Ellefson WL, Kashket ER (1987) Betaine transport imparts osmotolerance on a strain ofLactobacillus acidophilus. Appl Environ Microbiol 53:2275–2281

    Google Scholar 

  18. Kashket ER, Blanchard AG, Metzger WC (1980) Proton motive force during growth ofStreptococcus lactis cells. J Bacteriol 143:128–134

    PubMed  Google Scholar 

  19. Koujima I, Hayashi H, Tomochika K, Okabe A, Kanemasa Y (1978) Adaptational change in proline and water content ofStaphylococcus aureus after alteration of environmental salt concentration. Appl Environ Microbiol 35:467–470

    PubMed  Google Scholar 

  20. Le Rudulier D, Valentine RC (1982) Genetic engineering in agriculture: osmoregulation. Trends Biochem Sci 7:431–433

    Google Scholar 

  21. Le Rudulier D, Strom AR, Dandkar AM, Smith LT, Valentine RC (1984) Molecular biology of osmoregulation. Science 224:1064–1068

    Google Scholar 

  22. Measures JC (1975) Role of amino acids in osmoregulation of non-halophilic bacteria. Nature 257:398–400

    PubMed  Google Scholar 

  23. Minor TE, Marth EH (1976) Staphylococci and their significance in foods. New York: Elsevier Scientific Publishing

    Google Scholar 

  24. Pattee PA, Neveln DS (1975) Transformation analysis of three linkage groups inStaphylococcus aureus. J Bacteriol 124:201–211

    PubMed  Google Scholar 

  25. Riemann H, Bryan FL (1979) Food-borne infections and intoxications. New York: Academic Press

    Google Scholar 

  26. Smith JL, Buchanan RL, Palumbo SA (1983) Effect of food environment on staphylococcal enterotoxin synthesis: a review. J Food Prot 46:545–555

    Google Scholar 

  27. Troller JA (1986) Water relations of foodborne bacterial pathogens—an updated review. J Food Prot 49:656–670

    Google Scholar 

  28. Witter LD, Anderson CB (1987) Osmoregulation by microorganisms at reduced water activity. In: Montville TJ (ed) Food microbiology, vol. 1. Boca Raton, Florida: CRC Press, pp 1–34

    Google Scholar 

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Authors and Affiliations

  1. Department of Graduate Programs in Plant Physiology, The Pennsylvania State University, University Park, Pennsylvania, USA

    Karen J. Miller

  2. Department of Genetics, The Pennsylvania State University, University Park, Pennsylvania, USA

    Karen J. Miller

  3. Department of Food Science, The Pennsylvania State University, 111 Borland Laboratory, 16802, University Park, PA, USA

    Karen J. Miller, Susan C. Zelt & Ji-Hyun Bae

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  1. Karen J. Miller
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  2. Susan C. Zelt
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  3. Ji-Hyun Bae
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Miller, K.J., Zelt, S.C. & Bae, JH. Glycine betaine and proline are the principal compatible solutes ofStaphylococcus aureus . Current Microbiology 23, 131–137 (1991). https://doi.org/10.1007/BF02091971

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