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J. Biol. Chem., Vol. 281, Issue 16, 10778-10785, April 21, 2006

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The Gene ncgl2918 Encodes a Novel Maleylpyruvate Isomerase That Needs Mycothiol as Cofactor and Links Mycothiol Biosynthesis and Gentisate Assimilation in Corynebacterium glutamicum^*

Jie Feng¹, Yongsheng Che¹, Johanna Milse, Ya-Jie Yin^¶, Lei Liu^¶, Christian Rückert, Xi-Hui Shen, Su-Wei Qi, Jörn Kalinowski, and Shuang-Jiang Liu²

From the State Key Laboratory of Microbial Resources at Institute of Microbiology, Chinese Academy of Sciences, Beijing 100080, People's Republic of China, the Institut für Genomforschung, Universität Bielefeld, 33615 Bielefeld, Germany, and the ^¶Graduate School of Chinese Academy of Sciences, Beijing 100039, People's Republic of China

Data mining of the Corynebacterium glutamicum genome identified 4 genes analogous to the mshA, mshB, mshC, and mshD genes that are involved in biosynthesis of mycothiol in Mycobacterium tuberculosis and Mycobacterium smegmatis. Individual deletion of these genes was carried out in this study. Mutants mshC^– and mshD^– lost the ability to produce mycothiol, but mutant mshB^– produced mycothiol as the wild type did. The phenotypes of mutants mshC^– and mshD^– were the same as the wild type when grown in LB or BHIS media, but mutants mshC^– and mshD^– were not able to grow in mineral medium with gentisate or 3-hydroxybenzoate as carbon sources. C. glutamicum assimilated gentisate and 3-hydroxybenzoate via a glutathione-independent gentisate pathway. In this study it was found that the maleylpyruvate isomerase, which catalyzes the conversion of maleylpyruvate into fumarylpyruvate in the glutathione-independent gentisate pathway, needed mycothiol as a cofactor. This mycothiol-dependent maleylpyruvate isomerase gene (ncgl2918) was cloned, actively expressed, and purified from Escherichia coli. The purified mycothiol-dependent isomerase is a monomer of 34 kDa. The apparent K_m and V_max values for maleylpyruvate were determined to be 148.4 ± 11.9 µM and 1520 ± 57.4 µmol/min/mg, respectively (mycothiol concentration, 2.5 µM). Previous studies had shown that mycothiol played roles in detoxification of oxidative chemicals and antibiotics in streptomycetes and mycobacteria. To our knowledge, this is the first demonstration that mycothiol is essential for growth of C. glutamicum with gentisate or 3-hydroxybenzoate as carbon sources and the first characterization of a mycothiol-dependent maleylpyruvate isomerase.

Received for publication, December 12, 2005 , and in revised form, January 23, 2006.

^* This work was supported by National Natural Science Foundation of China Grant 30230010 and Chinese Academy of Sciences Grant KSCX2-SW-113. 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.

¹ Both authors contributed equally to this work.

² To whom correspondence should be addressed: Institute of Microbiology, Chinese Academy of Sciences, Zhong-Guan-Cun, Haidian, Beijing 100080, P. R. China. Tel.: 86-10-62527118; Fax: 86-10-62652317; E-mail: liusj{at}sun.im.ac.cn.

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