Skip to main content
SpringerLink
Log in

Application of nuclear magnetic resonance spectroscopy to analysis of ethanol fermentation kinetics in yeasts and bacteria

  • Published:
Biotechnology Letters Aims and scope Submit manuscript

Abstract

Nuclear Magnetic Resonance (NMR) spectroscopy is proving to be a very valuable technique for characterizing the metabolic status of a range of microbial fermentations. This non-invasive method allows us not only to determine the presence of particular metabolites, but also to monitor reaction rates, enzyme activities and transport mechanisms in vivo. Despite the low levels of the carbon-13 isotope (1.1%), natural-abundance 13C-NMR studies have proven useful in monitoring the progress of various fermentation processes. Furthermore, 31P-NMR can provide noninvasive information relating to cellular metabolism, and on the energy status of the cells. This results from the facility with NMR to identify various nucleotide phosphates and other energy-rich compounds in the cell, as well as to characterize changes in the intracellular pH from the chemical shifts of internal phosphate and other phosphorylated intermediates. In this review, we will summarize the use of NMR as an analytical tool in biotechnology and also discuss examples that illustrate how NMR can be used to obtain significant information on the characteristics of ethanol fermentations in both yeasts and bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bacher A, Rieder C, Eichinger D, Arigoni D, Fuchs G, Eisenrech W (1999) FEMS Microbiol. Rev. 22: 567–598.

    Google Scholar 

  • Bacic G, Ratkovic S (1987) J. Exp. Bot. 38: 1284–1297.

    Google Scholar 

  • Banuelos M, Gancedo C, Gancedo JM (1977) J. Biol. Chem. 252: 6394–6398.

    Google Scholar 

  • Barrow KD, Collins JG, Norton RS, Rogers PL, Smith GM (1984) J. Biol. Chem. 259: 5711–5716.

    Google Scholar 

  • Barrow KD, Rogers PL, Smith GM (1986) Eur. J. Biochem. 157:195–202.

    Google Scholar 

  • Bernstein MA, Hall LD, Hull WE (1979) J. Am. Chem. Soc. 101: 2744–2747.

    Google Scholar 

  • Björling T, Lindman B (1989) Enzyme Microbiol. Technol. 11: 240–246.

    Google Scholar 

  • Brindle KM, Brown FF, Campbell ID, Grathwohl C, Kuchel PW (1979) Biochem. J. 180: 37–44.

    Google Scholar 

  • Chandrakant P, Bisaria VS (1998) Crit. Rev. Biotechnol. 18: 295–331.

    Google Scholar 

  • Chu SC-K, Xu Y, Balschi JA, Springer CS Jr (1990) Magn. Reson. Med. 13: 239–262.

    Google Scholar 

  • de Graaf AA, Striegel K, Wittig RM, Laufer B, Schmitz G, Wiechert W, Sprenger GA, Sahm H (1999) Arch. Micobiol. 171: 371–385.

    Google Scholar 

  • den Hollander JA, Ugrubil K, Brown TR, Shulman RG (1981) Biochemistry 20: 5871–5880.

    Google Scholar 

  • den Hollander JA, Ugrubil K, Shulman RG (1986) Biochemistry 25: 212–219.

    Google Scholar 

  • Doelle HW, Kirk L, Crittenden R, Toh H, Doelle M (1983) Crit. Rev. Biotechnol. 13: 57–98.

    Google Scholar 

  • Dombek KM, Ingram LO (1986) Appl. Environ. Microbiol. 51: 197–200.

    Google Scholar 

  • Doran PM, Bailey JE (1986) Biotechnol. Bioeng. 28: 73–87.

    Google Scholar 

  • du Preez JC (1994) Enzyme Microbiol. Technol. 16: 944–956.

    Google Scholar 

  • Gadian DG (1995) Nuclear Magnetic Resonance and its Applications to Living Systems, 2nd edn. New York: Oxford University Press.

    Google Scholar 

  • Galazzo JL, Shanks JV, Bailey JE (1987) Biotechnol. Tech. 1: 1–6.

    Google Scholar 

  • Galazzo JL, Bailey JE (1989) Biotechnol. Bioeng. 33: 1283–1289.

    Google Scholar 

  • Galazzo JL, Bailey JE (1990) Biotechnol. Bioeng. 36: 417–426.

    Google Scholar 

  • Guijarro JM, Lagunas R (1984) J. Bacteriol. 160: 874–878.

    Google Scholar 

  • Hunter BK, Nicholls KM, Sanders JKM (1984) Biochemistry 23: 508–514.

    Google Scholar 

  • Ingram LO (1986) Trends Biotechnol. 2: 40–44.

    Google Scholar 

  • Joachimsthal E, Haggett KD, Jang J-H, Rogers PL (1998) Biotechnol. Lett. 20: 137–142.

    Google Scholar 

  • Joachimsthal E, Haggett KD, Rogers PL (1999) Appl. Biochem. Biotechnol. 77–79: 147–157.

    Google Scholar 

  • Jones RP (1989) Enzyme Microbiol. Technol. 11: 130–153.

    Google Scholar 

  • Karel SF, Libicki SB, Robertson CR (1985) Chem. Eng. Sci. 40: 1321–1354.

    Google Scholar 

  • Karel SE, Briasco CA, Robertson CR (1987) Ann. N.Y. Acad. Sci. 506: 84–104.

    Google Scholar 

  • Keifer PA (1999) Curr. Opin. Biotechnol. 10: 34–41.

    Google Scholar 

  • Kim IS, Barrow KD, Rogers, PL (1999a) Kinetic and NMR studies of xylose metabolism by recombinant Zymomonas mobilis ZM4 (pZB5) (submitted).

  • Kim IS, Barrow KD, Rogers, PL (1999b) In: Proceedings of the 21st Symposium on Biotechnology for Fuels and Chemicals, May 2–5, Fort Collins, CO, Abstr. 2–28.

  • Kim IS, Barrow KD, Rogers PL (1999c) In vivo NMR studies of ethanol fermentation characteristics and acetic acid inhibition of a recombinant Zymomonas mobilis ZM4 (pZB5) (submitted).

  • Lawford HG (1988) Appl. Microbiol. Biotechnol. 17: 203–219.

    Google Scholar 

  • Lawford HG, Stevnsborg N (1986) Biotechnol. Bioeng. Symp. 17: 209–219.

    Google Scholar 

  • Lawford HG, Rousseau JD (1993) Appl. Biochem. Biotechnol. 39/40: 301–322.

    Google Scholar 

  • Lawford HG, Rousseau JD (1999a) Appl. Biochem. Biotechnol. 77–79: 235–249.

    Google Scholar 

  • Lawford HG, Rousseau JD (1999b) In: Proceedings of the 21 st Symposium on Biotechnology for Fuels and Chemicals, May 2–5, Fort Collins, CO, Abstr. 2–24.

  • Lawford HG, Rousseau JD, Mohagheghi S, McMillan JD (1998) Appl. Biochem. Biotechnol. 70–72: 353–367.

    Google Scholar 

  • Lee J (1997) J. Biotechnol. 56: 1–24.

    Google Scholar 

  • Lee KJ, Skotnicki ML, Tribe DE, Rogers PL (1980) Biotechnol. Lett. 2: 339–334.

    Google Scholar 

  • Ligthelm ME, Prior BA, du Preez JC, Brandt V (1988) Appl. Microbiol. Biotechnol. 28: 293–296

    Google Scholar 

  • Lohmeier-Vogel EM, Hahn-Hägerdal B (1985) Appl. Microbiol. Biotechnol. 21: 167–172.

    Google Scholar 

  • Lohmeier-Vogel EM, Skoog K, Vogel H, Hahn-Hägerdal B (1989) Appl. Environ. Microbiol. 55: 1974–1980.

    Google Scholar 

  • Lohmeier-Vogel EM, McIntyre DD, Vogel HJ (1990) In: de Bont JAM, Visser J, Mattiasson B, Tramper J, eds. Physiology of Immobilized Cells. Amsterdam: Elsevier Science Publishers, pp. 661–676.

    Google Scholar 

  • Lohmeier-Vogel EM, Hahn-Hägerdal B, Vogel HJ (1995a) Appl. Environ. Microbiol. 61: 1414–1419.

    Google Scholar 

  • Lohmeier-Vogel EM, Hahn-Hägerdal B, Vogel HJ (1995b) Appl. Environ. Microbiol. 61: 1420–1425.

    Google Scholar 

  • Lohmeier-Vogel EM, McIntyre DD, Vogel HJ (1996) Appl. Environ. Microbiol. 62: 2832–2838.

    Google Scholar 

  • Lohmeier-Vogel EM, Sopher CR, Lee H (1998) J. Ind. Microbiol. Biotechnol. 20: 75–81.

    Google Scholar 

  • Loureiro-Dias M, Santos H (1990) Arch. Microbiol. 153: 384–391.

    Google Scholar 

  • Lundberg P, Harmsen E, Ho C, Vogel HJ (1990) Anal. Biochem. 191: 193–222.

    Google Scholar 

  • Maleszka R, Schneider H (1982) Can. J. Microbiol. 28: 360–363.

    Google Scholar 

  • Marx A, de Graaf AA, Wiechert W, Eggeling L, Sahm H (1996) Biotechnol. Bioeng. 49: 111–129.

    Google Scholar 

  • Marx A, Striegel K, de Graaf AA, Sahm H, Eggeling L (1997) Biotechnol. Bioeng. 56: 168–180.

    Google Scholar 

  • Nigam JN, Ireland RS, Margaritis A, Lachance MA (1985) Appl. Environ. Microbiol. 50: 1486–1489.

    Google Scholar 

  • Pamment NB (1989) In: van Uden N, ed. Alcohol Toxicity in Yeasts and Bacteria. Boca Raton, FL: CRC Press, Inc., pp. 1–76.

    Google Scholar 

  • Ranatunga TD, Jervis J, Helm RF, McMillan JD, Hatzis C (1997) Appl. Biochem. Biotechnol. 67: 185–198.

    Google Scholar 

  • Rogers PL, Lee KJ, Tribe DE (1979) Biotechnol. Lett. 1: 165–170.

    Google Scholar 

  • Rogers PL, Lee KJ, Skotnicki ML, Tribe DE (1982) Adv. Biochem. Engin. 23: 37–84.

    Google Scholar 

  • Sauer U, Hatzimanikatis V, Bailey JE, Hochuli M, Szyperski T, Wüthrich K (1997) Nature Biotechnol. 15: 448–452.

    Google Scholar 

  • Schoberth SM, de Graaf AA (1993) Anal. Biochem. 210: 123–128.

    Google Scholar 

  • Schoberth SM, Chapman BE, Kuthel PW, Wittig RM, Grotendorst J, Jansen P, de Graaf AA (1996) J. Bacteriol. 178: 1756–1761.

    Google Scholar 

  • Sonntag K, Schwinde J, de Graaf AA, Marx A, Eikmanns BJ, Wiechert W, Sahm H (1995) Appl. Microbiol. Biotechnol. 44: 489–495.

    Google Scholar 

  • Stein WD (1986). Transport and Diffusion Across Cell Membranes. New York: Academic Press.

    Google Scholar 

  • Strohhäcker J, de Graaf AA, Schoberth SM, Wittig RM, Sahm H (1993) Arch. Microbiol. 159: 484–490.

    Google Scholar 

  • Taipa MA, Cabral JMS, Santos H (1993) Biotechnol. Bioeng. 41: 647–653.

    Google Scholar 

  • Taylor KB, Beck MJ, Huang DH, Sakai TT (1990), J. Ind. Microbiol. 6: 29–41.

    Google Scholar 

  • Toivola A, Yarrow D, Van den Bosch E, Van Dijken JP, Scheffers, WA (1984) Appl. Environ. Microbiol. 47: 1221–1223.

    Google Scholar 

  • van Uden N (1989) In: van Uden N, ed. Alcohol Toxicity in Yeasts and Bacteria. Boca Raton, FL: CRC Press, Inc, pp. 135–146.

    Google Scholar 

  • Vogel HJ (1987) Ann. New York Acad. Sci. 508: 164–175.

    Google Scholar 

  • Vogel HJ, Brodelius P, Lilja H, Lohmeier-Vogel EM (1987) Methods Enzymol. 135: 512–528.

    Google Scholar 

  • Zhang M, Eddy C, Deanda K, Finkelstein M, Picataggio S (1995) Science 67: 240–243.

    Google Scholar 

  • Zhang M, Chou YG, Lai XK, Mistrey S, Danielson N, Evans K, Mohagheghi A, Finkelstein M (1999) Proceedings of 21 st Symposium Biotechnology for Fuels and Chemicals, May 2–5, Fort Collins, CO, Abstr. 2–16.

Download references

Author information

Authors and Affiliations

  1. Department of Biotechnology, Australia

    In Seop Kim & Peter L. Rogers

  2. School of Biochemistry and Molecular Genetics, University of New South Wales, Sydney, Australia, 2052

    Kevin D. Barrow

Authors
  1. In Seop Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kevin D. Barrow
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter L. Rogers
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, I.S., Barrow, K.D. & Rogers, P.L. Application of nuclear magnetic resonance spectroscopy to analysis of ethanol fermentation kinetics in yeasts and bacteria. Biotechnology Letters 21, 839–848 (1999). https://doi.org/10.1023/A:1005519323748

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1005519323748

Search

Navigation