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J. Biol. Chem., Vol. 279, Issue 17, 17810-17818, April 23, 2004

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A Novel Cyanobacterial SmtB/ArsR Family Repressor Regulates the Expression of a CPx-ATPase and a Metallothionein in Response to Both Cu(I)/Ag(I) and Zn(II)/Cd(II)^*

Tong Liu, Susumu Nakashima¶, Kazunobu Hirose, Mineo Shibasaka, Maki Katsuhara, Bunichi Ezaki, David P. Giedroc, and Kunihiro Kasamo||

From the Research Institute for Bioresources, Okayama University, Kurashiki, Okayama 710-0046, Japan and the Department of Biochemistry and Biophysics, Texas A&M University, College Station, Texas 77843-2128

A novel SmtB/ArsR family metalloregulator, denoted BxmR, has been identified and characterized from the cyanobacterium Oscillatoria brevis. Genetic and biochemical evidence reveals that BxmR represses the expression of both bxa1, encoding a CPx-ATPase metal transporter, as well as a divergently transcribed operon encoding bxmR and bmtA, a heavy metal sequestering metallothionein. Derepression of the expression of all three genes is mediated by both monovalent (Ag(I) and Cu(I)) and divalent (Zn(II) and Cd(II)) heavy metal ions, a novel property among SmtB/ArsR metal sensors. Electrophoretic gel mobility shift experiments reveal that apoBxmR forms multiple resolvable complexes with oligonucleotides containing a single 12-2-12 inverted repeat derived from one of the two operator/promoter regions with similar apparent affinities. Preincubation with either monovalent or divalent metal ions induces disassembly of both the BxmR-bxa1 and BxmR-bxmR/bmtA operator/promoter complexes. Interestingly, the temporal regulation of expression of bxa1 and bmtA mRNAs is different in O. brevis with bxa1 induced first upon heavy metal treatment, followed by bmtA/bxmR. A dynamic interplay among Bxa1, BmtA, and BxmR is proposed that maintains metal homeostasis in O. brevis by balancing the relative rates of metal storage and efflux of multiple heavy metal ions.

Received for publication, September 24, 2003 , and in revised form, February 10, 2004.

The nucleotide sequence(s) reported in this paper has been submitted to the DDBJ/GenBank^TM/EBI Data Bank with accession number(s) AB085750, AB085749, and AB073990.

^* This work was supported in part by grants from the Sumitomo Foundation (to S. N.), the Oohara Foundation for Agricultural Sciences, Grant-in-aid for the Future Program from the Japanese Society for the Promotion of Science 9616001 (to S. N.), Grants for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology of Japan 11440237 (to K K.) and 10878087 (to S. N.), and National Institutes of Health Grant GM042569 (to D. P. G.). 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.

^¶ To whom correspondence may be addressed. Tel.: 81-86-434-1211; Fax: 81-86-434-1249; E-mail: snakashi{at}rib.okayama-u.ac.jp.

^|| To whom correspondence may be addressed. Tel.: 979-845-4231; Fax: 979-845-4946; E-mail: giedroc{at}tamu.edu.

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