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J. Biol. Chem., Vol. 283, Issue 5, 2684-2692, February 1, 2008

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Identification of Two Homologous Genes, chlA_I and chlA_II, That Are Differentially Involved in Isocyclic Ring Formation of Chlorophyll a in the Cyanobacterium Synechocystis sp. PCC 6803^*

Kei Minamizaki, Tadashi Mizoguchi, Takeaki Goto, Hitoshi Tamiaki, and Yuichi Fujita¹

From the Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan and the Department of Bioscience and Biotechnology, Ritsumeikan University, Kusatsu 525-8577, Japan

The isocyclic ring (E-ring) is a common structural feature of chlorophylls. The E-ring is formed by two structurally unrelated Mg-protoporphyrin IX monomethylester (MPE) cyclase systems, oxygen-dependent (AcsF), and oxygen-independent (BchE) systems, which involve incorporation of an oxygen atom from molecular oxygen and water into the C-13¹ position of MPE, respectively. Which system operates in cyanobacteria that can thrive in a variety of anaerobic environments remains an open question. The cyanobacterium Synechocystis sp. PCC 6803 has two acsF-like genes, sll1214 (chlA_I) and sll1874 (chlA_II), and three bchE-like genes, slr0905, sll1242, and slr0309. Five mutants lacking one of these genes were isolated. The chlA_I mutant failed to grow under aerobic conditions with anomalous accumulation of a pigment with fluorescence emission peak at 595 nm, which was identified 3,8-divinyl MPE by high-performance liquid chromatography-mass spectrometry analysis. The growth defect of chlA_I was restored by the cultivation under oxygen-limited (micro-oxic) conditions. MPE accumulation was also detected in chlA_II grown under microoxic conditions, but not in any of the bchE mutants. The phenotype was consistent with the expression pattern of two chlA genes: chlA_II was induced under micro-oxic conditions in contrast to the constitutive expression of chlA_I. These findings suggested that ChlA_I is the sole MPE cyclase system under aerobic conditions and that the induced ChlA_II operates together with ChlA_I under micro-oxic conditions. In addition, the accumulation of 3,8-divinyl MPE in the chlA mutants suggested that the reduction of 8-vinyl group occurs after the formation of E-ring in Synechocystis sp. PCC 6803.

Received for publication, October 31, 2007 , and in revised form, November 20, 2007.

^* This work was supported in part by a Grant-in-Aid for Scientific Research (Grant nos. 19570036, 15570033, 13CE2005, and 14COEA2), Toyoaki Scholarship Foundation and The Japan Securities Scholarship Foundation (to Y. F.), and the Academic Frontier Project for Private Universities, a matching fund subsidy from the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of the Japanese Government, 2003–2007 (to H. T.), and by Grants-in-Aid for Scientific Research (B) for Young Scientists (Number 19750148) (to T. M.) from Japan Society for the Promotion of Science. 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 supplemental Table S1 and Figs. S1 and S2.

¹ To whom correspondence should be addressed: Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, Japan. Tel.: 81-52-789-4105; Fax: 81-52-789-4107; E-mail: fujita{at}agr.nagoya-u.ac.jp.

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