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Applied and Environmental Microbiology, October 2004, p. 5778-5786, Vol. 70, No. 10
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.10.5778-5786.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Stable-Isotope Probing of Microorganisms Thriving at Thermodynamic Limits: Syntrophic Propionate Oxidation in Flooded Soil

Tillmann Lueders,{dagger} Bianca Pommerenke, and Michael W. Friedrich*

Max Planck Institute for Terrestrial Microbiology, Marburg, Germany

Received 18 February 2004/ Accepted 9 June 2004

Propionate is an important intermediate of the degradation of organic matter in many anoxic environments. In methanogenic environments, due to thermodynamic constraints, the oxidation of propionate requires syntrophic cooperation of propionate-fermenting proton-reducing bacteria and H2-consuming methanogens. We have identified here microorganisms that were active in syntrophic propionate oxidation in anoxic paddy soil by rRNA-based stable-isotope probing (SIP). After 7 weeks of incubation with [13C]propionate (<10 mM) and the oxidation of ~30 µmol of 13C-labeled substrate per g dry weight of soil, we found that archaeal nucleic acids were 13C labeled to a larger extent than those of the bacterial partners. Nevertheless, both terminal restriction fragment length polymorphism and cloning analyses revealed Syntrophobacter spp., Smithella spp., and the novel Pelotomaculum spp. to predominate in "heavy" 13C-labeled bacterial rRNA, clearly showing that these were active in situ in syntrophic propionate oxidation. Among the Archaea, mostly Methanobacterium and Methanosarcina spp. and also members of the yet-uncultured "rice cluster I" lineage had incorporated substantial amounts of 13C label, suggesting that these methanogens were directly involved in syntrophic associations and/or thriving on the [13C]acetate released by the syntrophs. With this first application of SIP in an anoxic soil environment, we were able to clearly demonstrate that even guilds of microorganisms growing under thermodynamic constraints, as well as phylogenetically diverse syntrophic associations, can be identified by using SIP. This approach holds great promise for determining the structure and function relationships of further syntrophic or other nutritional associations in natural environments and for defining metabolic functions of yet-uncultivated microorganisms.

* Corresponding author. Mailing address: Department of Biogeochemistry, Max Planck Institute for Terrestrial Microbiology, Karl-von-Frisch Strasse, D-35043 Marburg, Germany. Phone: 49-6421-178830. Fax: 49-6421-178809. E-mail: michael.friedrich{at}staff.uni-marburg.de.

{dagger} Present address: Institute of Groundwater Ecology, GSF-National Research Center for Environment and Health, Ingolstaedter Landstr. 1, D-85764 Neuherberg, Germany.

Applied and Environmental Microbiology, October 2004, p. 5778-5786, Vol. 70, No. 10
0099-2240/04/$08.00+0     DOI: 10.1128/AEM.70.10.5778-5786.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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