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Originally published In Press as doi:10.1074/jbc.M112468200 on March 19, 2002

J. Biol. Chem., Vol. 277, Issue 21, 18658-18664, May 24, 2002
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Genes Essential to Sodium-dependent Bicarbonate Transport in Cyanobacteria
FUNCTION AND PHYLOGENETIC ANALYSIS*

Mari ShibataDagger , Hirokazu KatohDagger , Masatoshi SonodaDagger , Hiroshi OhkawaDagger , Masaya ShimoyamaDagger , Hideya Fukuzawa§, Aaron Kaplan, and Teruo OgawaDagger ||

From the Dagger  Bioscience Center, Nagoya University, Chikusa, Nagoya 464-8601, Japan, the § Graduate School of Biostudies, Kyoto University, Sakyo, Kyoto 606-8502, Japan, and the  Department of Plant Sciences, Hebrew University, 91904 Jerusalem, Israel

The cyanobacterium Synechocystis sp. strain PCC 6803 possesses two CO2 uptake systems and two HCO<UP><SUB>3</SUB><SUP>−</SUP></UP> transporters. We transformed a mutant impaired in CO2 uptake and in cmpA-D encoding a HCO<UP><SUB>3</SUB><SUP>−</SUP></UP>transporter with a transposon inactivation library, and we recovered mutants unable to take up HCO<UP><SUB>3</SUB><SUP>−</SUP></UP> and grow in low CO2 at pH 9.0. They are all tagged within slr1512 (designated sbtA). We show that SbtA-mediated transport is induced by low CO2, requires Na+, and plays the major role in HCO<UP><SUB>3</SUB><SUP>−</SUP></UP> uptake in Synechocystis. Inactivation of slr1509 (homologous to ntpJ encoding a Na+/K+-translocating protein) abolished the ability of cells to grow at [Na+] higher than 100 mM and severely depressed the activity of the SbtA-mediated HCO<UP><SUB>3</SUB><SUP>−</SUP></UP> transport. We propose that the SbtA-mediated HCO<UP><SUB>3</SUB><SUP>−</SUP></UP> transport is driven by Delta µNa+ across the plasma membrane, which is disrupted by inactivating ntpJ. Phylogenetic analyses indicated that two types of sbtA exist in various cyanobacterial strains, all of which possess ntpJ. The sbtA gene is the first one identified as essential to Na+-dependent HCO<UP><SUB>3</SUB><SUP>−</SUP></UP> transport in photosynthetic organisms and may play a crucial role in carbon acquisition when CO2 supply is limited, or in Prochlorococcus strains that do not possess CO2 uptake systems or Cmp-dependent HCO<UP><SUB>3</SUB><SUP>−</SUP></UP> transport.

* This work was supported by Grant-in-aid for Scientific Research B 2-12440228, by Human Frontier Science Program Grant RG0051/1997M (to T. O.), by Grant-in-aid for Scientific Research 12660300 (to H. F.), by Research for the Future Grant JSPS-RFTF97R16001 (to T.O. and H. F.), from the Japan Society for the Promotion of Science, by a grant from the USA-Israel Binational Science Foundation (to A. K.), and by a grant from Program MARS2 (a cooperation of the German Ministerium für Bildung, Wissenschaft, Forschung und Technologie and the Israeli Ministry of Science and Technology) (to A. K.).The costs of publication of this article were defrayed in part by the payment of page charges. The 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. Tel.: 81-52-789-5215; Fax: 81-52-789-5214; E-mail: ogawater@agr.nagoya-u.ac.jp.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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