Previous Article | Next Article 
Journal of Bacteriology, September 2009, p. 5793-5801, Vol. 191, No. 18
0021-9193/09/$08.00+0 doi:10.1128/JB.00356-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
The Electron Transfer System of Syntrophically Grown Desulfovibrio vulgaris
,
Christopher B. Walker,1,8,
Zhili He,2,3,8
Zamin K. Yang,2,8
Joseph A. Ringbauer Jr.,4,8
Qiang He,2,8
Jizhong Zhou,2,3,8
Gerrit Voordouw,5
Judy D. Wall,4,8
Adam P. Arkin,6,7,8
Terry C. Hazen,7,8
Sergey Stolyar,1,8 and
David A. Stahl1,8*
Department of Civil and Environmental Engineering, University of Washington, Seattle, Washington,1 Biosciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee,2 Institute For Environmental Genomics and Department of Botany and Microbiology, University of Oklahoma, Norman, Oklahoma,3 Biochemistry Division and Molecular Microbiology and Immunology Department, University of Missouri, Columbia, Missouri,4 Department of Biological Sciences, University of Calgary, Calgary, Alberta, Canada,5 Department of Bioengineering, University of California, Berkeley, California,6 Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California,7 Virtual Institute for Microbial Stress and Survival, Lawrence Berkeley National Laboratory, Berkeley, California8
Received 13 March 2009/ Accepted 29 June 2009
Interspecies hydrogen transfer between organisms producing and consuming hydrogen promotes the decomposition of organic matter in most anoxic environments. Although syntrophic coupling between hydrogen producers and consumers is a major feature of the carbon cycle, mechanisms for energy recovery at the extremely low free energies of reactions typical of these anaerobic communities have not been established. In this study, comparative transcriptional analysis of a model sulfate-reducing microbe, Desulfovibrio vulgaris Hildenborough, suggested the use of alternative electron transfer systems dependent on growth modality. During syntrophic growth on lactate with a hydrogenotrophic methanogen, numerous genes involved in electron transfer and energy generation were upregulated in D. vulgaris compared with their expression in sulfate-limited monocultures. In particular, genes coding for the putative membrane-bound Coo hydrogenase, two periplasmic hydrogenases (Hyd and Hyn), and the well-characterized high-molecular-weight cytochrome (Hmc) were among the most highly expressed and upregulated genes. Additionally, a predicted operon containing genes involved in lactate transport and oxidation exhibited upregulation, further suggesting an alternative pathway for electrons derived from lactate oxidation during syntrophic growth. Mutations in a subset of genes coding for Coo, Hmc, Hyd, and Hyn impaired or severely limited syntrophic growth but had little effect on growth via sulfate respiration. These results demonstrate that syntrophic growth and sulfate respiration use largely independent energy generation pathways and imply that to understand microbial processes that sustain nutrient cycling, lifestyles not captured in pure culture must be considered.
* Corresponding author. Mailing address: Department of Civil and Environmental Engineering, University of Washington, 302 More Hall, Box 352700. Seattle, WA 98195-2700. Phone: (206) 685-3464. Fax: (206) 685-9185. E-mail: dastahl{at}u.washington.edu
Published ahead of print on 6 July 2009.
Supplemental material for this article may be found at http://jb.asm.org/.
Present address: Geosyntec Consultants, 1370 Stewart Avenue, Suite 205, Seattle, WA 98104.
Journal of Bacteriology, September 2009, p. 5793-5801, Vol. 191, No. 18
0021-9193/09/$08.00+0 doi:10.1128/JB.00356-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
Copyright © 2009 by the American Society for Microbiology. For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»