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Journal of Bacteriology, March 2006, p. 2115-2125, Vol. 188, No. 6
0021-9193/06/$08.00+0     doi:10.1128/JB.188.6.2115-2125.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Transcriptional and Biochemical Analysis of Starch Metabolism in the Hyperthermophilic Archaeon Pyrococcus furiosus

Han-Seung Lee,1 Keith R. Shockley,2 Gerrit J. Schut,1 Shannon B. Conners,2 Clemente I. Montero,2 Matthew R. Johnson,2 Chung-Jung Chou,2 Stephanie L. Bridger,2 Nathan Wigner,2 Scott D. Brehm,1 Francis E. Jenney Jr.,1 Donald A. Comfort,2 Robert M. Kelly,2 and Michael W. W. Adams1*

Department of Biochemistry and Molecular Biology, University of Georgia, Athens, Georgia 30602-7229,1 Department of Chemical and Biomolecular Engineering, North Carolina State University, Raleigh, North Carolina 27695-79052

Received 8 July 2005/ Accepted 16 December 2005

Pyrococcus furiosus utilizes starch and its degradation products, such as maltose, as primary carbon sources, but the pathways by which these {alpha}-glucans are processed have yet to be defined. For example, its genome contains genes proposed to encode five amylolytic enzymes (including a cyclodextrin glucanotransferase [CGTase] and amylopullulanase), as well as two transporters for maltose and maltodextrins (Mal-I and Mal-II), and a range of intracellular enzymes have been purified that reportedly metabolize maltodextrins and maltose. However, precisely which of these enzymes are involved in starch processing is not clear. In this study, starch metabolism in P. furiosus was examined by biochemical analyses in conjunction with global transcriptional response data for cells grown on a variety of glucans. In addition, DNA sequencing led to the correction of two key errors in the genome sequence, and these change the predicted properties of amylopullulanase (now designated PF1935*) and CGTase (PF0478*). Based on all of these data, a pathway is proposed that is specific for starch utilization that involves one transporter (Mal-II [PF1933 to PF1939]) and only three enzymes, amylopullulanase (PF1935*), 4-{alpha}-glucanotransferase (PF0272), and maltodextrin phosphorylase (PF1535). Their expression is upregulated on starch, and together they generate glucose and glucose-1-phosphate, which then feed into the novel glycolytic pathway of this organism. In addition, the results indicate that several hypothetical proteins encoded by three gene clusters are also involved in the transport and processing of {alpha}-glucan substrates by P. furiosus.

* Corresponding author. Mailing address: Department of Biochemistry and Molecular Biology, Davison Life Science Complex, Green St., University of Georgia, Athens, GA 30602-7229. Phone: (706) 542-2060. Fax: (706) 542-0229. E-mail: adams{at}bmb.uga.edu.

Journal of Bacteriology, March 2006, p. 2115-2125, Vol. 188, No. 6
0021-9193/06/$08.00+0     doi:10.1128/JB.188.6.2115-2125.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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