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Originally published In Press as doi:10.1074/jbc.M211748200 on December 9, 2002

J. Biol. Chem., Vol. 278, Issue 9, 7540-7552, February 28, 2003
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Carbohydrate-induced Differential Gene Expression Patterns in the Hyperthermophilic Bacterium Thermotoga maritima*,

Swapnil R. ChhabraDagger , Keith R. ShockleyDagger , Shannon B. ConnersDagger , Kevin L. Scott§, Russell D. Wolfinger§, and Robert M. KellyDagger

From the Dagger  Department of Chemical Engineering, North Carolina State University, Raleigh, North Carolina 27695 and § SAS Institute Inc., Cary, North Carolina 27513

The hyperthermophilic bacterium Thermotoga maritima MSB8 was grown on a variety of carbohydrates to determine the influence of carbon and energy source on differential gene expression. Despite the fact that T. maritima has been phylogenetically characterized as a primitive microorganism from an evolutionary perspective, results here suggest that it has versatile and discriminating mechanisms for regulating and effecting complex carbohydrate utilization. Growth of T. maritima on monosaccharides was found to be slower than growth on polysaccharides, although growth to cell densities of 108 to 109 cells/ml was observed on all carbohydrates tested. Differential expression of genes encoding carbohydrate-active proteins encoded in the T. maritima genome was followed using a targeted cDNA microarray in conjunction with mixed model statistical analysis. Coordinated regulation of genes responding to specific carbohydrates was noted. Although glucose generally repressed expression of all glycoside hydrolase genes, other sugars induced or repressed these genes to varying extents. Expression profiles of most endo-acting glycoside hydrolase genes correlated well with their reported biochemical properties, although exo-acting glycoside hydrolase genes displayed less specific expression patterns. Genes encoding selected putative ABC sugar transporters were found to respond to specific carbohydrates, and in some cases putative oligopeptide transporter genes were also found to respond to specific sugar substrates. Several genes encoding putative transcriptional regulators were expressed during growth on specific sugars, thus suggesting functional assignments. The transcriptional response of T. maritima to specific carbohydrate growth substrates indicated that sugar backbone- and linkage-specific regulatory networks are operational in this organism during the uptake and utilization of carbohydrate substrates. Furthermore, the wide ranging collection of such networks in T. maritima suggests that this organism is capable of adapting to a variety of growth environments containing carbohydrate growth substrates.


* This work was supported in part by grants from the National Science Foundation (NSF) Biotechnology Program, an NSF IGERT Traineeship (to S. B. C.), and the Department of Energy Energy Biosciences Program.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains two additional tables.

To whom correspondence should be addressed: Dept. of Chemical Engineering, North Carolina State University, 113 Riddick Lab, Box 7905, Raleigh, NC 27695-7905. Tel.: 919-515-6396; Fax: 919-515-3465; E-mail: rmkelly@eos.ncsu.edu.


Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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