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Applied and Environmental Microbiology, November 2007, p. 6842-6853, Vol. 73, No. 21
0099-2240/07/$08.00+0     doi:10.1128/AEM.00597-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Impact of Substrate Glycoside Linkage and Elemental Sulfur on Bioenergetics of and Hydrogen Production by the Hyperthermophilic Archaeon Pyrococcus furiosus{triangledown} ,{dagger}

Chung-Jung Chou,1 Keith R. Shockley,1,{ddagger} Shannon B. Conners,1,§ Derrick L. Lewis,1 Donald A. Comfort,1,¶ Michael W. W. Adams,2 and Robert M. Kelly1*

Department of Chemical and Biomolecular Engineering, North Carolina State University, Raleigh, North Carolina 27695-7905,1 Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia 30602-72292

Received 15 March 2007/ Accepted 26 August 2007

Glycoside linkage (cellobiose versus maltose) dramatically influenced bioenergetics to different extents and by different mechanisms in the hyperthermophilic archaeon Pyrococcus furiosus when it was grown in continuous culture at a dilution rate of 0.45 h–1 at 90°C. In the absence of S0, cellobiose-grown cells generated twice as much protein and had 50%-higher specific H2 generation rates than maltose-grown cultures. Addition of S0 to maltose-grown cultures boosted cell protein production fourfold and shifted gas production completely from H2 to H2S. In contrast, the presence of S0 in cellobiose-grown cells caused only a 1.3-fold increase in protein production and an incomplete shift from H2 to H2S production, with 2.5 times more H2 than H2S formed. Transcriptional response analysis revealed that many genes and operons known to be involved in {alpha}- or ß-glucan uptake and processing were up-regulated in an S0-independent manner. Most differentially transcribed open reading frames (ORFs) responding to S0 in cellobiose-grown cells also responded to S0 in maltose-grown cells; these ORFs included ORFs encoding a membrane-bound oxidoreductase complex (MBX) and two hypothetical proteins (PF2025 and PF2026). However, additional genes (242 genes; 108 genes were up-regulated and 134 genes were down-regulated) were differentially transcribed when S0 was present in the medium of maltose-grown cells, indicating that there were different cellular responses to the two sugars. These results indicate that carbohydrate characteristics (e.g., glycoside linkage) have a major impact on S0 metabolism and hydrogen production in P. furiosus. Furthermore, such issues need to be considered in designing and implementing metabolic strategies for production of biofuel by fermentative anaerobes.

* Corresponding author. Mailing address: Department of Chemical and Biomolecular Engineering, North Carolina State University, EB-1, 911 Partners Way, Raleigh, NC 27695-7905. Phone: (919) 515-6396. Fax: (919) 515-3465. E-mail: rmkelly{at}eos.ncsu.edu

{triangledown} Published ahead of print on 7 September 2007.

{dagger} Supplemental material for this article may be found at http://aem.asm.org/.

{ddagger} Present address: The Jackson Laboratory, 600 Main Street, Bar Harbor, ME 04609.

§ Present address: SAS Institute, Cary, NC.

Present address: Wyeth Pharmaceuticals, Sanford, NC.

Applied and Environmental Microbiology, November 2007, p. 6842-6853, Vol. 73, No. 21
0099-2240/07/$08.00+0     doi:10.1128/AEM.00597-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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