Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Anaerobic microbial metabolism can proceed close to thermodynamic limits

Abstract

Many fermentative bacteria obtain energy for growth by reactions in which the change in free energy (ΔG′) is less than that needed to synthesize ATP1,2,3,4. These bacteria couple substrate metabolism directly to ATP synthesis, however, by classical phosphoryl transfer reactions4,5. An explanation for the energy economy of these organisms is that biological systems conserve energy in discrete amounts3,4, with a minimum, biochemically convertible energy value of about -20 kJ mol-1 (refs 1, 2, 3). This concept predicts that anaerobic substrate decay ceases before the minimum free energy value is reached, and several studies support this prediction1,6,7,8,9. Here we show that metabolism by syntrophic associations, in which the degradation of a substrate by one species is thermodynamically possible only through removal of the end product by another species1, can occur at values close to thermodynamic equilibrium (ΔG′ ≈ 0 kJ mol-1). The free energy remaining when substrate metabolism halts is not constant; it depends on the terminal electron-accepting reaction and the amount of energy required for substrate activation. Syntrophic associations metabolize near thermodynamic equilibrium, indicating that bacteria operate extremely efficient catabolic systems.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Schink, B. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol. Mol. Biol. Rev. 61, 262–280 (1997).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Schink, B. in Biotechnology, Focus 2 (eds Finn, R. K. & Präve, P.) 63–89 (Hanser, Munich, 1990).

    Google Scholar 

  3. Schink, B. & Thauer, R. in Granular Anaerobic Sludge: Microbiology and Technology (eds Lettinga, G. et al.) 5–17 (Pudoc, Wageningen, 1988).

    Google Scholar 

  4. Thauer, R. K. & Morris, J. G. Metabolism of chemotrophic anaerobes: old views and new aspects. Symf. Soc. Gen. Microbiol. 36, 123–168 (1984).

    Google Scholar 

  5. Thauer, R. K., Jungermann, K. & Decker, K. Energy conservation in chemotrophic anaerobic bacteria. Bacteriol. Rev. 41, 100–180 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Kleerebezem, R. & Stams, A. J. M. Kinetics of syntrophic cultures: A theoretical treatise on butyrate fermentation. Biotechnol. Bioeng. 67, 529–543 (2000).

    Article  CAS  PubMed  Google Scholar 

  7. Warikoo, V., McInerney, M. J., Robinson, J. A. & Suflita, J. M. Interspecies acetate transfer influences the extent of anaerobic benzoate degradation by syntrophic consortia. Appl. Environ. Microbiol. 62, 26–32 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Schöcke, L. & Schink, B. Energetics of methanogenic benzoate degradation by Syntrophus gentianae in syntrophic coculture. Microbiology 143, 2345–2351 (1997).

    Article  PubMed  Google Scholar 

  9. Christensen, T. H. et al. Characterization of redox conditions in groundwater contaminant plumes. J. Contam. Hydrol. 45, 165–241 (2000).

    Article  ADS  CAS  Google Scholar 

  10. Coutts, D. A. P., Senior, E. & Balba, M. T. M. Multi-stage chemostat investigation of interspecies interactions in a hexanoate-catabolizing microbial association isolated from anoxic landfill. J. Appl. Bacteriol. 62, 731–740 (1987).

    Article  Google Scholar 

  11. Dojka, M. A., Hugenholtz, P., Haack, S. K. & Pace, N. R. Microbial diversity in a hydrocarbon- and chlorinated-solvent-contaminated aquifer undergoing intrinsic bioremediation. Appl. Environ. Microbiol. 64, 3869–3877 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. McInerney, M. J. & Bryant, M. P. in Biomass Conversion Processes for Energy and Fuels (eds Sofer, S. S. & Zaborsky, O. R.) 277–296 (Plenum, New York, 1981).

    Book  Google Scholar 

  13. Jackson, B. E. Thermodynamics and energetics of syntrophic substrate degradation. Thesis, Univ. Oklahoma (1999).

  14. Harwood, C. S., Burchardt, G., Hermann, H. & Fuchs, G. Anaerobic metabolism of aromatic compounds via the benzoyl-CoA pathway. FEMS Microbiol. Rev. 22, 439–458 (1999).

    Article  Google Scholar 

  15. Seitz, H.-J., Schink, B., Pfennig, N. & Conrad, R. Energetics of syntrophic ethanol oxidation in defined chemostat cocultures 1. Energy requirement for H2 production and H2 oxidation. Arch. Microbiol. 155, 82–88 (1990).

    Article  CAS  Google Scholar 

  16. Dwyer, D. F., Weeg-Aerssens, E., Shelton, D. R. & Teidje, J. M. Bioenergetic conditions of butyrate metabolism by a syntrophic, anaerobic bacterium in coculture with hydrogen-oxidizing methanogenic and sulfidogenic bacteria. Appl. Environ. Microbiol. 54, 1354–1359 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Scholten, J. C. M. & Conrad, R. Energetics of syntrophic propionate oxidation in defined batch and chemostat cocultures. Appl. Environ. Microbiol. 66, 2934–2942 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Auburger, G. & Winter, J. Purification and characterization of the benzoyl-CoA ligase from a syntrophic, benzoate-degrading anaerobic mixed culture. Appl. Microbiol. Biotechnol. 37, 789–795 (1992).

    Article  CAS  PubMed  Google Scholar 

  19. Elshahed, M. S., Bhupathiraju, V. K., Wofford, N. Q., Nanny, M. A. & McInerney, M. J. Metabolism of benzoate, cyclohex-1-ene carboxylate and cyclohexane carboxylate by Syntrophus aciditrophicus strain SB in syntrophic association with H2-using microorganisms. Appl. Environ. Microbiol. 67, 1728–1738 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Harwood, C. S. & Gibson, J. Shedding light on anaerobic benzene ring degradation: a process unique to prokaryotes? J. Bacteriol. 179, 301–309 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wofford, N. Q., Beaty, P. S. & McInerney, M. J. Preparation of cell-free extracts and the enzymes involved in fatty acid metabolism in Syntrophomonas wolfei. J. Bacteriol. 167, 179–185 (1986).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Tran, Q. H. & Unden, G. Changes in the proton potential and the cellular energetics of Escherichia coli during growth by aerobic and anaerobic respiration or by fermentation. Eur. J. Biochem. 251, 538–543 (1998).

    Article  CAS  PubMed  Google Scholar 

  23. Jetten, M. S. M., Stams, A. J. M. & Zehnder, A. J. B. Adenine nucleotide content and energy charge of Methanothrix soehngenii during acetate degradation. FEMS Microbiol. Lett. 84, 313–318 (1991).

    Article  CAS  Google Scholar 

  24. Maloney, P. Relationship between phosphorylation potential and electrochemical H+ gradient during glycolysis in Streptococcus lactis. J. Bacteriol. 153, 1461–1470 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Cramer, W. A. & Knaff, D. B. Energy Transduction in Biological Membranes: a Textbook of Bioenergetics (Springer, New York, 1990).

    Book  Google Scholar 

  26. Stock, D., Leslie, A. G. W. & Walker, J. E. Molecular architecture of the rotary motor in ATP synthase. Science 286, 1700–1705 (1999).

    Article  CAS  PubMed  Google Scholar 

  27. Balch, W. E. & Wolfe, R. S. New approach to the cultivation of methanogenic bacteria: 2-mercaptoethanesulfonic acid (HS-CoM)-dependent growth of Methanobacterium ruminantium in a pressurized atmosphere. Appl. Environ. Microbiol. 32, 781–791 (1976).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. McInerney, M. J., Bryant, M. P. & Pfennig, N. An anaerobic bacterium that degrades fatty acids in syntrophic association with methanogens. Arch. Microbiol. 122, 129–135 (1979).

    Article  CAS  Google Scholar 

  29. Seiler, W., Giehl, H. & Roggendorf, P. Detection of carbon monoxide and hydrogen by conversion of mercury oxide to mercury vapor. Atmos. Technol. 12, 40–45 (1980).

    Google Scholar 

  30. Kaiser, J. L. & Hanselmann, K. W. Fermentative metabolism of substituted monoaromatic compounds by a bacterial community from anaerobic sediments. Arch. Microbiol. 133, 384–391 (1982).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the US Department of Energy.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael J. McInerney.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jackson, B., McInerney, M. Anaerobic microbial metabolism can proceed close to thermodynamic limits. Nature 415, 454–456 (2002). https://doi.org/10.1038/415454a

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/415454a

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing