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Appl Environ Microbiol. 1988 June; 54(6): 1354-1359
Copyright © 1988, American Society for Microbiology. All Rights Reserved.

Bioenergetic Conditions of Butyrate Metabolism by a Syntrophic, Anaerobic Bacterium in Coculture with Hydrogen-Oxidizing Methanogenic and Sulfidogenic Bacteria

Daryl F. Dwyer, Els Weeg-Aerssens, Daniel R. Shelton^|| and James M. Tiedje^*

¹ Departments of Microbiology and Public Health and Crop and Soil Science, ² Michigan State University, East Lansing, Michigan 48824

ABSTRACT

The butyrate-oxidizing, proton-reducing, obligately anaerobic bacterium NSF-2 was grown in batch cocultures with either the hydrogen-oxidizing bacterium Methanospirillum hungatei PM-1 or Desulfovibrio sp. strain PS-1. Metabolism of butyrate occurred in two phases. The first phase exhibited exponential growth kinetics (phase a) and had a doubling time of 10 h. This value was independent of whether NSF-2 was cultured with a methanogen or a sulfate reducer and likely represents the maximum specific growth rate of NSF-2. This exponential growth phase was followed by a second phase with a nearly constant rate of degradation (phase b) which dominated the time course of butyrate degradation. The specific activity of H₂ uptake by the hydrogen-oxidizing bacterium controlled the bioenergetic conditions of metabolism in phase b. During this phase both the Gibbs free energy (G') and the butyrate degradation rate (v) were greater for NSF-2-Desulfovibrio sp. strain PS-1 (G' = –17.0 kJ/mol; v = 0.20 mM/h) than for NSF-2-M. hungatei PM-1 (G' = –3.8 kJ/mol, v = 0.12 mM/h). The G' value remained stable and characteristic of the two hydrogen oxidizers during phase b. The stable G' resulted from the close coupling of the rates of butyrate and H₂ oxidation. The addition of 2-bromoethanesulfonate to a NSF-2-methanogen coculture resulted in the total inhibition of butyrate degradation; the inhibition was relieved when Desulfovibrio sp. strain PS-1 was added as a new H₂ sink. When the specific activity of H₂ consumption was increased by adding higher densities of the Desulfovibrio sp. to 2-bromoethanesulfonate-inhibited NSF-2-methanogen cocultures, lower H₂ pool sizes and higher rates of butyrate degradation resulted. Thus, it is the kinetic parameters of H₂ consumption, not the type of H₂ consumer per se, that establishes the thermodynamic conditions which in turn control the rate of fatty acid degradation. The bioenergetic homeostasis we observed in phase b was a result of the kinetics of the coculture members and the feedback inhibition by hydrogen which prevents butyrate degradation rates from reaching their theoretical V_max.

^* Corresponding author.

Present address: Department of Medical Biochemistry, University of Geneva, CH-1211 Geneva 4, Switzerland.

Present address: Procter and Gamble ETC, Temselaan 100, B-1820 Strombeek-Bever, Belgium.

^|| Present address: Pesticide Degradation Laboratory, BARC-West, Beltsville, MD 20705.

Journal article no. 12509 of the Michigan Agricultural Experiment Station.

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