Skip to main content
Log in

Growth yields and energy generation by Campylobacter sputorum subspecies bubulus during growth in continuous culture with different hydrogen acceptors

  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

Campylobacter sputorum subspecies bubulus was grown in continuous culture with excess of l-lactate or formate, and growth-limiting amounts of oxygen, fumarate, nitrate or nitrite. l-Lactate was oxidized to acetate, fumarate was reduced to succinate, and nitrate and nitrite were reduced to ammonia. The Y lactate values (g dry weight bacteria/g mol lactate) for the respective hydrogen acceptors were much higher than the Y formate values. Steady state cultures on formate and nitrite could only be obtained at a low dilution rate and low nitrite concentrations in the growth medium. In →H+/2e measurements with lactate-grown cells proton ejections were observed with lactate or pyruvate as a hydrogen donor, and oxygen or hydrogen peroxide as a hydrogen acceptor. Proton ejection was also observed with pyruvate and nitrate. Proton ejection did not occur with lactate and nitrate, neither with lactate or pyruvate and fumarate or nitrite. With formate as a hydrogen donor acidification occurred with all hydrogen acceptors mentioned. It has been concluded that during growth on lactate and fumarate or nitrite substrate level phosphorylation at acetate formation is the sole ATP-generating system. Growth on formate and fumarate or nitrite is explained by a proton gradient generated as a result of oxidation of formate at the periplasmic side of the cytoplasmic membrane. With oxygen and nitrate additional ATP is formed by electron transport-linked phosphorylation. The low molar growth yields with formate are explained by the observation that formate-grown cells had a great permeability to protons.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

→ H+/2e value:

number of protons ejected per electron pair transported in the respiratory system

P/2e value:

mol of ATP formed per electron pair transported in the respiratory system

CCCP:

carbonyl cyanide m-chlorophenyl-hydrazone

References

  • Bernhard, T., Gottschalk, G.: Cell yields of Escherichia coli during anaerobic growth on fumarate and molecular hydrogen. Arch. Microbiol. 116, 235–238 (1978)

    Google Scholar 

  • Cole, J. A.: The rapid accumulation of large quantities of ammonia during nitrite reduction by Escherichia coli. FEMS Microbiol. Lett. 4, 327–329 (1978)

    Google Scholar 

  • Da Fonseca-Wollheim, F.: Direkte Plasmaammoniakbestimmung ohne Enteiweißung. Z. Klin. Chem. Klin. Biochem. 11, 426–431 (1973)

    Google Scholar 

  • Hadjipetrou, L. P., Stouthamer, A. H.: Energy production during nitrate respiration by Aerobacter aerogenes. J. Gen. Microbiol. 38, 29–34 (1965)

    Google Scholar 

  • Hasan, S. M., Hall, J. B.: The physiological function of nitrate reduction in Clostridum perfringens. J. Gen. Microbiol. 87, 120–128 (1975)

    Google Scholar 

  • Inderlied, C. B., Delwiche, E. A.: Nitrate reduction and the growth of Veillonella alcalescens. J. Bacteriol. 114, 1206–1212 (1973)

    Google Scholar 

  • Kröger, A.: Phosphorylative electron transport with fumarate and nitrate as terminal hydrogen acceptors. Symposium 27 of the Society for General Microbiology (B. A. Haddock, W. A. Hamilton, eds.), pp. 61–93. London, New York, Melbourne: Cambridge University Press 1977

    Google Scholar 

  • Laanbroek, H. J., Stal, L. J., Veldkamp, H.: Utilization of hydrogen and formate by Campylobacter spec. under aerobic and anaerobic conditions. Arch. Microbiol. 119, 99–102 (1978)

    Google Scholar 

  • Laanbroek, H. J., Veldkamp, H.: Growth yield and energy generation in anaerobically-grown Campylobacter spec. Arch. Microbiol. 120, 47–51 (1979)

    Google Scholar 

  • Lang, E., Lang, H.: Spezifische Farbreaktion zum direkten Nachweis der Ameisensäure. Z. Anal. Chemie 260, 8–10 (1972)

    Google Scholar 

  • Linton, J. D., Griffiths, K., Harrison, D. E. F., Bull, A. T.: Growth of Beneckea natriegens on mixtures of glucose and formate in chemostat culture. Soc. Gen. Microbiol. Quarterly 6, 91 (1979)

    Google Scholar 

  • Meyer, E. M., van Verseveld, H. W., van der Beek, E. G., Stouthamer, A. H.: Energy conservation during aerobic growth in Paracoccus denitrificans. Arch. Microbiol. 112, 25–34 (1977)

    Google Scholar 

  • Meyer, E. M., van der Zwaan, J. W., Wever, R., Stouthamer, A. H.: Anaerobic respiration and energy conservation in Paracoccus denitrificans. Functioning of iron-sulfur centers and the uncoupling effect of nitrite. Eur. J. Biochem. 96, 69–76 (1979)

    Google Scholar 

  • Mitchell, P., Moyle, J.: Respiration driven proton translocation in rat liver mitochondria. Biochem. J. 105, 1147–1162 (1967)

    Google Scholar 

  • Niederman, R. A., Wolin, M. J.: Requirement of succinate for the growth of Vibrio succinogenes. J. Bacteriol. 109, 546–549 (1972)

    Google Scholar 

  • Niekus, H. G. D., de Vries, W., Stouthamer, A. H.: The effect of different dissolved oxygen tensions on growth and enzyme activities of Campylobacter sputorum subspecies bubulus. J. Gen. Microbiol. 103, 215–222 (1977)

    Google Scholar 

  • Niekus, H. G. D., Wouters, C. H., de Vries, W., Stouthamer, A. H.: Superoxide dismutase and hydrogen peroxide formation in Campylobacter sputorum subspecies bubulus. Arch. Microbiol. 119, 37–42 (1978)

    Google Scholar 

  • van Palenstein Helderman, W. H., Rosman, J.: Hydrogen —dependent organisms from the human gingival crevice resembling Vibrio succinogenes. Antonie van Leeuwenhoek J. Microbiol. Serol. 42, 107–118 (1976)

    Google Scholar 

  • Pirt, S. J., Callow, D. S.: Exocellular product formation by microorganisms in continuous culture. I. Production of 2,3-butanediol by Aerobacter aerogenes in a single stage process. J. Appl. Bacteriol. 21, 188–205 (1958)

    Google Scholar 

  • Scholes, P. B., Mitchell, P.: Respiration — driven proton translocation in Micrococcus denitrificans. J. Bioenerg. 1, 309–323 (1970)

    Google Scholar 

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

    Google Scholar 

  • van Verseveld, H. W., Meyer, E. M., Stouthmer, A. H.: Energy conservation during nitrate respiration in Paracoccus denitrificans. Arch. Microbiol. 112, 17–23 (1977)

    Google Scholar 

  • de Vries, W., Stouthamer, A. H.: Fermentation of glucose, lactose, galactose, mannitol and xylose by bifidobacteria. J. Bacteriol. 96, 472–478 (1968)

    Google Scholar 

  • de Vries, W., Rietveld-Struyk, T. R. M., Stouthamer, A. H.: ATP formation associated with fumarate and nitrate reduction in growing cultures of Veillonella alcalescens. Antonie van Leeuwenhoek J. Microbiol. Serol. 43, 153–167 (1977)

    Google Scholar 

  • Wood, P. M.: A chemiosmotic model for sulphate respiration. FEBS Lett. 95, 12–18 (1978)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

de Vries, W., Niekus, H.G.D., Boellaard, M. et al. Growth yields and energy generation by Campylobacter sputorum subspecies bubulus during growth in continuous culture with different hydrogen acceptors. Arch. Microbiol. 124, 221–227 (1980). https://doi.org/10.1007/BF00427730

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00427730

Key words

Navigation