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Journal of Bacteriology, December 2005, p. 8020-8025, Vol. 187, No. 23
0021-9193/05/$08.00+0     doi:10.1128/JB.187.23.8020-8025.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Decaprenylphosphoryl Arabinofuranose, the Donor of the D-Arabinofuranosyl Residues of Mycobacterial Arabinan, Is Formed via a Two-Step Epimerization of Decaprenylphosphoryl Ribose

Katarína Mikuová,^1, Hairong Huang,^2, Tetsuya Yagi,³ Marcelle Holsters,⁴ Danny Vereecke,⁴ Wim D'Haeze, Michael S. Scherman,² Patrick J. Brennan,² Michael R. McNeil,² and Dean C. Crick^2*

Department of Biochemistry, Faculty of Natural Sciences, Comenius University, Bratislava, Slovakia,¹ Mycobacteria Research Laboratories, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado,² Division of Respiratory Medicine, National Center for Geriatrics and Gerontology, Obu, Aichi, Japan,³ Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology, Ghent University, B-9052 Ghent, Belgium⁴

Received 6 June 2005/ Accepted 21 September 2005

The major cell wall polysaccharide of mycobacteria is a branched-chain arabinogalactan in which arabinan chains are attached to the 5 carbon of some of the 6-linked galactofuranose residues; these arabinan chains are composed exclusively of D-arabinofuranose (Araf) residues. The immediate precursor of the polymerized Araf is decaprenylphosphoryl-D-Araf, which is derived from 5-phosphoribose 1-diphosphate (pRpp) in an undefined manner. On the basis of time course, feedback, and chemical reduction experiment results we propose that decaprenylphosphoryl-Araf is synthesized by the following sequence of events. (i) pRpp is transferred to a decaprenyl-phosphate molecule to form decaprenylphosphoryl-ß-D-5-phosphoribose. (ii) Decaprenylphosphoryl-ß-D-5-phosphoribose is dephosphorylated to form decaprenylphosphoryl-ß-D-ribose. (iii) The hydroxyl group at the 2 position of the ribose is oxidized and is likely to form decaprenylphosphoryl-2-keto-ß-D-erythro-pentofuranose. (iv) Decaprenylphosphoryl-2-keto-ß-D-erythro-pentofuranose is reduced to form decaprenylphosphoryl-ß-D-Araf. Thus, the epimerization of the ribosyl to an arabinosyl residue occurs at the lipid-linked level; this is the first report of an epimerase that utilizes a lipid-linked sugar as a substrate. On the basis of similarity to proteins implicated in the arabinosylation of the Azorhizobium caulidans nodulation factor, two genes were cloned from the Mycobacterium tuberculosis genome and expressed in a heterologous host, and the protein was purified. Together, these proteins (Rv3790 and Rv3791) are able to catalyze the epimerization, although neither protein individually is sufficient to support the activity.

K.M. and H.H. contributed equally to the work reported here.

Present address: The Scripps Research Institute, Chemistry Department, 10550 North Torrey Pines Road, La Jolla, CA.

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