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J. Biol. Chem., Vol. 279, Issue 6, 4330-4338, February 6, 2004

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Isolation and Functional Characterization of Ca²⁺/H⁺ Antiporters from Cyanobacteria^*

Rungaroon Waditee, Gazi Sakir Hossain, Yoshito Tanaka, Tatsunosuke Nakamura¶, Masamitsu Shikata||, Jun Takano||, Tetsuko Takabe**, and Teruhiro Takabe

From the Research Institute, and Graduate School of Environmental and Human Sciences, Meijo University, Nagoya, 468-8502, ^¶Faculty of Pharmacy, Niigata University of Pharmacy and Applied Life Science, Niigata, 950-2081, ^||Shimadzu Co. Nakagyou-ku, Kyoto, 604-8511, and ^**Graduate School of Agricultural Science, Nagoya University, Chikusa-ku, Nagoya, 464-8601, Japan

Genome sequences of cyanobacteria, Synechocystis sp. PCC 6803, Anabaena sp. PCC 7120, and Thermosynechococcus elongatus BP-1 revealed the presence of a single Ca²⁺/H⁺ antiporter in these organisms. Here, we isolated the putative Ca²⁺/H⁺ antiporter gene from Synechocystis sp. PCC 6803 (synCAX) as well as a homologous gene from a halotolerant cyanobacterium Aphanothece halophytica (apCAX). In contrast to plant vacuolar CAXs, the full-length apCAX and synCAX genes complemented the Ca²⁺-sensitive phenotype of an Escherichia coli mutant. ApCAX and SynCAX proteins catalyzed specifically the Ca²⁺/H⁺ exchange reaction at alkaline pH. Immunological analysis suggested their localization in plasma membranes. The Synechocystis sp. PCC 6803 cells disrupted of synCAX exhibited lower Ca²⁺ efflux activity and a salt-sensitive phenotype. Overexpression of ApCAX and SynCAX enhanced the salt tolerance of Synechococcus sp. PCC 7942 cells. Mutagenesis analyses indicate the importance of two conserved acidic amino acid residues, Glu-74 and Glu-324, in the transmembrane segments for the exchange activity. These results clearly indicate that cyanobacteria contain a Ca²⁺/H⁺ antiporter in their plasma membranes, which plays an important role for salt tolerance.

Received for publication, September 16, 2003 , and in revised form, October 13, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the DDBJ/GenBank^TM/EBI Data Bank with accession number(s) AB120300.

^* This work was supported in part by grants-in-aid for Scientific Research from the Ministry of Education and Science and Culture of Japan, the High-Tech Research Center of Meijo University. 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 should be addressed: Research Institute of Meijo University, Tenpaku-ku, Nagoya, Aichi 468-8502, Japan. Tel.: 81-52-832-1151; Fax: 81-52-832-1545; E-mail: takabe{at}ccmfs.meijo-u.ac.jp.

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