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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
Carbohydrate-induced Differential Gene Expression Patterns in
the Hyperthermophilic Bacterium Thermotoga
maritima*,
Swapnil R.
Chhabra ,
Keith R.
Shockley ,
Shannon B.
Conners ,
Kevin L.
Scott§,
Russell D.
Wolfinger§, and
Robert M.
Kelly ¶
From the 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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