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J. Biol. Chem., Vol. 281, Issue 13, 8450-8457, March 31, 2006

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Differentiation of Carbazole Catabolic Operons by Replacement of the Regulated Promoter via Transposition of an Insertion Sequence^*

From the Biotechnology Research Center, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-8657, Japan

The carbazole catabolic car operons from Pseudomonas resinovorans CA10 and Janthinobacterium sp. J3 have nearly identical nucleotide sequences in their structural and intergenic regions but not in their flanking regions. Transposition of ISPre1 from the anthranilate catabolic ant operon located an inducible promoter P_ant upstream of the car_CA10 operon, which is regulated by the AraC/XylS family activator AntR in response to anthranilate. The transposed P_ant drives transcription of the car_CA10 operon, which is composed of the car-AaAaBaBbCAcAdDFE_CA10 structural genes. Transcriptional fusion truncating P_ant upstream of carAa_CA10 resulted in constitutive luciferase expression. Primer extension analysis identified a transcription start point of the constitutive mRNA of the car_CA10 operon at 385 nucleotides upstream of the carAa_CA10 translation start point, and the P_carAa promoter was found. On the other hand, a GntR family regulatory gene carR_J3 is divergently located upstream of the car_J3 operon. The P_u13 promoter, required for inducible transcription of the car_J3 operon in the presence of carbazole, was identified in the region upstream of carAa_J3, which had been replaced with the P_ant promoter in the car_CA10 operon. Deletion of carR_J3 from a transcriptional fusion resulted in high level constitutive expression from P_u13. Purified CarR_J3 protein bound at two operator sequences O_I and O_II, showing that CarR_J3 directly represses P_u13 in the absence of its inducer, which was identified as 2-hydroxy-6-oxo-6-(2'-aminophenyl)hexa-2,4-dienoate, an intermediate of the carbazole degradation pathway.

Received for publication, January 10, 2006 , and in revised form, January 31, 2006.

^* This work was supported in part by a Grant-in-Aid for Scientific Research (13660080) (to H. N.) from the Ministry of Education, Science, Sports, and Culture of Japan. 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 Fig. S1 and Tables S1 and S2.

¹ Supported by Research fellowships of the Japan Society for the Promotion of Science for Young Scientists.

² Present address: Dept. of Industrial Chemistry, Shibaura Institute of Technology, 3-9-14 Shibaura, Minato-ku, Tokyo 108-8548, Japan.

³ To whom correspondence should be addressed. Tel.: 81-3-5841-3064; Fax: 81-3-5841-8030; E-mail: anojiri{at}mail.ecc.u-tokyo.ac.jp.

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