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Applied and Environmental Microbiology, March 2006, p. 2080-2091, Vol. 72, No. 3
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.3.2080-2091.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Non-Sulfate-Reducing, Syntrophic Bacteria Affiliated with Desulfotomaculum Cluster I Are Widely Distributed in Methanogenic Environments

Hiroyuki Imachi,1* Yuji Sekiguchi,1,2 Yoichi Kamagata,1,2 Alexander Loy,3 Yan-Ling Qiu,1,2 Philip Hugenholtz,4 Nobutada Kimura,2 Michael Wagner,3 Akiyoshi Ohashi,1 and Hideki Harada1

Department of Environmental Systems Engineering, Nagaoka University of Technology, Nagaoka, Niigata 940-2188, Japan,1 Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST) Center 6, Tsukuba, Ibaraki 305-8566, Japan,2 Department of Microbial Ecology, University of Vienna, A-1090 Vienna, Austria,3 Microbial Ecology Program, DOE Joint Genome Institute, Walnut Creek, California4

Received 16 November 2005/ Accepted 27 December 2005

The classical perception of members of the gram-positive Desulfotomaculum cluster I as sulfate-reducing bacteria was recently challenged by the isolation of new representatives lacking the ability for anaerobic sulfate respiration. For example, the two described syntrophic propionate-oxidizing species of the genus Pelotomaculum form the novel Desulfotomaculum subcluster Ih. In the present study, we applied a polyphasic approach by using cultivation-independent and culturing techniques in order to further characterize the occurrence, abundance, and physiological properties of subcluster Ih bacteria in low-sulfate, methanogenic environments. 16S rRNA (gene)-based cloning, quantitative fluorescence in situ hybridization, and real-time PCR analyses showed that the subcluster Ih population composed a considerable part of the Desulfotomaculum cluster I community in almost all samples examined. Additionally, five propionate-degrading syntrophic enrichments of subcluster Ih bacteria were successfully established, from one of which the new strain MGP was isolated in coculture with a hydrogenotrophic methanogen. None of the cultures analyzed, including previously described Pelotomaculum species and strain MGP, consumed sulfite, sulfate, or organosulfonates. In accordance with these phenotypic observations, a PCR-based screening for dsrAB (key genes of the sulfate respiration pathway encoding the alpha and beta subunits of the dissimilatory sulfite reductase) of all enrichments/(co)cultures was negative with one exception. Surprisingly, strain MGP contained dsrAB, which were transcribed in the presence and absence of sulfate. Based on these and previous findings, we hypothesize that members of Desulfotomaculum subcluster Ih have recently adopted a syntrophic lifestyle to thrive in low-sulfate, methanogenic environments and thus have lost their ancestral ability for dissimilatory sulfate/sulfite reduction.

* Corresponding author. Mailing address: Department of Environmental Systems Engineering, Nagaoka University of Technology, 1603-1 Kamitomioka, Nagaoka, Niigata 940-2188, Japan. Phone: 81-258-47-9642. Fax: 81-258-47-9642. E-mail: imachi{at}vos.nagaokaut.ac.jp.

Applied and Environmental Microbiology, March 2006, p. 2080-2091, Vol. 72, No. 3
0099-2240/06/$08.00+0     doi:10.1128/AEM.72.3.2080-2091.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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