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J. Biol. Chem., Vol. 279, Issue 52, 54952-54962, December 24, 2004

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Na⁺-dependent K⁺ Uptake Ktr System from the Cyanobacterium Synechocystis sp. PCC 6803 and Its Role in the Early Phases of Cell Adaptation to Hyperosmotic Shock^*

Nobuyuki Matsuda, Hiroshi Kobayashi, Hirokazu Katoh, Teruo Ogawa, Lui Futatsugi, Tatsunosuke Nakamura¶, Evert P. Bakker||, and Nobuyuki Uozumi**

From the Bioscience and Biotechnology Center, Nagoya University, Nagoya 464-8601, Japan, the Graduate School of Pharmaceutical Sciences, Chiba University, 1-8-1, Inohana, Chuo-ku, Chiba 260-8675, Japan, the ^¶Faculty of Pharmacy, Niigata University of Pharmacy and Applied Life Sciences, Niigata 950-2081, Japan, and ^||Abteilung Mikrobiologie, Universität Osnabrück, Barbarastrasse 11, D-49076 Osnabrück, Germany

Transmembrane ion transport processes play a key role in the adaptation of cells to hyperosmotic conditions. Previous work has shown that the disruption of a ktrB/ntpJ-like putative Na⁺/K⁺ transporter gene in the cyanobacterium Synechocystis sp. PCC 6803 confers increased Na⁺ sensitivity, and inhibits uptake. Here, we report on the mechanistic basis of this effect. Heterologous expression experiments in Escherichia coli show that three Synechocystis genes are required for K⁺ transport activity. They encode an NAD⁺-binding peripheral membrane protein (ktrA; sll0493), an integral membrane protein, belonging to a superfamily of K⁺ transporters (ktrB; formerly ntpJ; slr1509), and a novel type of ktr gene product, not previously found in Ktr systems (ktrE; slr1508). In E. coli, Synechocystis KtrABE-mediated K⁺ uptake occurred with a moderately high affinity (K_m of about 60 µM), and depended on both Na⁺ and a high membrane potential, but not on ATP. KtrABE neither mediated Na⁺ uptake nor Na⁺ efflux. In Synechocystis sp. PCC 6803, KtrB-mediated K⁺ uptake required Na⁺ and was inhibited by protonophore. A ktrB strain was sensitive to long term hyperosmotic stress elicited by either NaCl or sorbitol. Hyperosmotic shock led initially to loss of net K⁺ from the cells. The ktrB cells shocked with sorbitol failed to reaccumulate K⁺ up to its original level. These data indicate that in strain PCC 6803 K⁺ uptake via KtrABE plays a crucial role in the early phase of cell turgor regulation after hyperosmotic shock.

Received for publication, June 29, 2004 , and in revised form, September 20, 2004.

^* This work was supported by a grant-in-aid for Center of Excellence (COE) Research (to N. U.), the 21st Century COE Program (to N. U.), Grants-in-aid for Scientific Research (15380070, 15902677, and 16013219; to N. U.) from the Ministry of Education, Science, Sports and Culture of Japan, and grants from the Japan Society for the Promotion of Science Research of the Future Program (to N. U.). 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: Bioscience and Biotechnology Center, Nagoya University, Nagoya 464-8601, Japan. Tel.: 81-52-789-5202; Fax: 81-52-789-5206; E-mail: uozumi{at}agr.nagoya-u.ac.jp.

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