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J. Biol. Chem., Vol. 281, Issue 40, 29872-29885, October 6, 2006

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Comparative Genomics and Experimental Characterization of N-Acetylglucosamine Utilization Pathway of Shewanella oneidensis^*

Chen Yang¹, Dmitry A. Rodionov¹², Xiaoqing Li, Olga N. Laikova^¶, Mikhail S. Gelfand^||, Olga P. Zagnitko^**, Margaret F. Romine³, Anna Y. Obraztsova, Kenneth H. Nealson³, and Andrei L. Osterman^**

From the Burnham Institute for Medical Research, La Jolla, California 92037, Institute for Information Transmission Problems, Russian Academy of Sciences, Moscow 127994, Russia, ^¶State Scientific Center GosNIIGenetika, Moscow 117545, Russia, ^||Department of Bioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia, ^**Fellowship for Interpretation of Genomes, Burr Ridge, Illinois 60527, Pacific Northwest National Laboratory, Richland, Washington 99352, and Department of Earth Sciences, University of Southern California, Los Angeles, California 90089

We used a comparative genomics approach implemented in the SEED annotation environment to reconstruct the chitin and GlcNAc utilization subsystem and regulatory network in most proteobacteria, including 11 species of Shewanella with completely sequenced genomes. Comparative analysis of candidate regulatory sites allowed us to characterize three different GlcNAc-specific regulons, NagC, NagR, and NagQ, in various proteobacteria and to tentatively assign a number of novel genes with specific functional roles, in particular new GlcNAc-related transport systems, to this subsystem. Genes SO3506 and SO3507, originally annotated as hypothetical in Shewanella oneidensis MR-1, were suggested to encode novel variants of GlcN-6-P deaminase and GlcNAc kinase, respectively. Reconstitution of the GlcNAc catabolic pathway in vitro using these purified recombinant proteins and GlcNAc-6-P deacetylase (SO3505) validated the entire pathway. Kinetic characterization of GlcN-6-P deaminase demonstrated that it is the subject of allosteric activation by GlcNAc-6-P. Consistent with genomic data, all tested Shewanella strains except S. frigidimarina, which lacked representative genes for the GlcNAc metabolism, were capable of utilizing GlcNAc as the sole source of carbon and energy. This study expands the range of carbon substrates utilized by Shewanella spp., unambiguously identifies several genes involved in chitin metabolism, and describes a novel variant of the classical three-step biochemical conversion of GlcNAc to fructose 6-phosphate first described in Escherichia coli.

Received for publication, May 26, 2006 , and in revised form, July 20, 2006.

^* This work was supported in part by NIAID Grant 1-R01-AI059146-01A2 from the National Institutes of Health (to A. L. O.), Howard Hughes Medical Institute Grant 55005610 (to M. S. G.), Russian Academy of Sciences Program "Molecular and Cellular Biology" (to D. A. R. and M. S. G.), Russian Fund of Basic Research Grant 04-04-49361 (to D. A. R.), and INTAS Grant 05-8028 (to M. S. G. and D. A. R.). The costs of publication of this article were defrayed in part by the payment of page charges. This 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 supplemental Tables S1, S2, S3, and S4.

¹ Both authors contributed equally to this work.

³ Supported by the Dept. of Energy Office of Biological and Environmental Sciences under the Genomics-GTL Program via the Shewanella Federation consortium.

² To whom correspondence should be addressed: Burnham Institute for Medical Research, 10901 N. Torrey Pines Rd., La Jolla, CA 92037. Tel.: 858-646-3100; Fax: 858-713-9949; E-mail: rodionov{at}burnham.org.

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