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Evidence for chemiosmotic coupling of reductive dechlorination and ATP synthesis in Desulfomonile tiedjei

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Abstract

Desulfomonile tiedjei (strain DCB-1) was previously shown to conserve energy for growth from reductive dechlorination of 3-chlorobenzoate coupled to formate oxidation. We tested the hypothesis that a chemiosmotic mechanism couples reductive dechlorination and ATP synthesis in D. tiedjei. Dechlorination resulted in an increase in the ATP pool of cells. Uncouplers and ionophores decreased both the dechlorination rate and the ATP pool. However, at low concentrations the inhibitors had relatively greater effects on the ATP pool, and in some cases, even appeared to stimulate dechlorination. Those agents could not completely inhibit ATP synthesis while allowing dechlorination activity. The proton-driven ATPase inhibitor, N,N′-dicyclohexylcarbodiimide (DCCD), had similar effects. An imposed pH gradient also resulted in an increase in the ATP pool of cells, and this increase was partially inhibited by DCCD. Addition of 3-chlorobenzoate to cell suspensions caused proton translocation by the cells. Proton translocation was stimulated by the permeant thiocyanate anion and inhibited by uncouplers. A maximum H+/3-chlorobenzoate ratio of greater than two was observed. These findings suggest that dechlorination supports formation of a proton-motive force which in turn supports ATP synthesis via a proton-driven ATPase.

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Abbreviations

3CB:

3-chlorobenzoate

CCCP:

m-chlorophenyl-hydrazone

DCCD:

N,N′-dicyclohexylcarbodiimide

DNP:

2,4-dinitrophenol

ΔP:

proton-motive force

PCP:

pentachlorophenol

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Author notes

  1. William W. Mohn

    Present address: Institute for Biological Sciences, National Research Council Canada, K1A OR6, Ottawa, Ontario, Canada

Authors and Affiliations

  1. Department of Microbiology, Michigan State University, 48824, East Lansing, MI, USA

    William W. Mohn & James M. Tiedje

  2. Department of Crop and Soil Sciences, Michigan State University, 48824, East Lansing, MI, USA

    James M. Tiedje

Authors
  1. William W. Mohn
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  2. James M. Tiedje
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Mohn, W.W., Tiedje, J.M. Evidence for chemiosmotic coupling of reductive dechlorination and ATP synthesis in Desulfomonile tiedjei . Arch. Microbiol. 157, 1–6 (1991). https://doi.org/10.1007/BF00245326

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  • DOI: https://doi.org/10.1007/BF00245326

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