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Applied and Environmental Microbiology, February 2007, p. 1153-1165, Vol. 73, No. 4
0099-2240/07/$08.00+0     doi:10.1128/AEM.01588-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Hydrogen Metabolism in Shewanella oneidensis MR-1{triangledown}

Galit Meshulam-Simon,1 Sebastian Behrens,1 Alexander D. Choo,2 and Alfred M. Spormann1,2,3*

Departments of Civil and Environmental Engineering,1 Biological Sciences,2 Geological and Environmental Sciences, Stanford University, Stanford, California 94305-54293

Received 9 July 2006/ Accepted 24 November 2006

Shewanella oneidensis MR-1 is a facultative sediment microorganism which uses diverse compounds, such as oxygen and fumarate, as well as insoluble Fe(III) and Mn(IV) as electron acceptors. The electron donor spectrum is more limited and includes metabolic end products of primary fermenting bacteria, such as lactate, formate, and hydrogen. While the utilization of hydrogen as an electron donor has been described previously, we report here the formation of hydrogen from pyruvate under anaerobic, stationary-phase conditions in the absence of an external electron acceptor. Genes for the two S. oneidensis MR-1 hydrogenases, hydA, encoding a periplasmic [Fe-Fe] hydrogenase, and hyaB, encoding a periplasmic [Ni-Fe] hydrogenase, were found to be expressed only under anaerobic conditions during early exponential growth and into stationary-phase growth. Analyses of {Delta}hydA, {Delta}hyaB, and {Delta}hydA {Delta}hyaB in-frame-deletion mutants indicated that HydA functions primarily as a hydrogen-forming hydrogenase while HyaB has a bifunctional role and represents the dominant hydrogenase activity under the experimental conditions tested. Based on results from physiological and genetic experiments, we propose that hydrogen is formed from pyruvate by multiple parallel pathways, one pathway involving formate as an intermediate, pyruvate-formate lyase, and formate-hydrogen lyase, comprised of HydA hydrogenase and formate dehydrogenase, and a formate-independent pathway involving pyruvate dehydrogenase. A reverse electron transport chain is potentially involved in a formate-hydrogen lyase-independent pathway. While pyruvate does not support a fermentative mode of growth in this microorganism, pyruvate, in the absence of an electron acceptor, increased cell viability in anaerobic, stationary-phase cultures, suggesting a role in the survival of S. oneidensis MR-1 under stationary-phase conditions.

* Corresponding author. Mailing address: Department of Civil and Environmental Engineering, Clark Center East Wing, 318 Campus Dr., E250A, Stanford University, Stanford, CA 94305-5429. Phone: (650) 723-3668. Fax: (650) 725-3164. E-mail: spormann{at}stanford.edu.

{triangledown} Published ahead of print on 22 December 2006.

Applied and Environmental Microbiology, February 2007, p. 1153-1165, Vol. 73, No. 4
0099-2240/07/$08.00+0     doi:10.1128/AEM.01588-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Lupa, B., Hendrickson, E. L., Leigh, J. A., Whitman, W. B. (2008). Formate-Dependent H2 Production by the Mesophilic Methanogen Methanococcus maripaludis. Appl. Environ. Microbiol. 74: 6584-6590 [Abstract] [Full Text]  
  • Dolfing, J., Jiang, B., Henstra, A. M., Stams, A. J. M., Plugge, C. M. (2008). Syntrophic Growth on Formate: a New Microbial Niche in Anoxic Environments. Appl. Environ. Microbiol. 74: 6126-6131 [Abstract] [Full Text]  


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