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J. Biol. Chem., Vol. 278, Issue 22, 19939-19946, May 30, 2003

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A Two-component System Mediates Developmental Regulation of Biosynthesis of a Heterocyst Polysaccharide^*

Ruanbao Zhou   and C. Peter Wolk  ¶ ||

From the MSU-DOE Plant Research Laboratory and the ^¶Department of Plant Biology, Michigan State University, East Lansing, Michigan 48824

Some cyanobacteria couple oxygenic photosynthesis in vegetative cells with O₂-sensitive N₂ fixation in differentiated cells called heterocysts. Heterocyst differentiation involves extensive biochemical and structural changes that collectively permit heterocysts to assimilate N₂ aerobically and supply the products of N₂ fixation to vegetative cells. HepK and DevR are required for the development of functional heterocysts in Anabaena and Nostoc, respectively. We show that HepK is an autokinase and that Anabaena DevR_A is its cognate response regulator, together comprising part or all of a two-component system that mediates developmental regulation of biosynthesis of a heterocyst envelope polysaccharide. Recombinant N-hexahistidine-tagged HepK (H₆HepK), the cytoplasmic portion H₆'HepK of H₆HepK, H₆DevR, and H₆DevR_A were overexpressed in Escherichia coli and purified to homogeneity. H₆'HepK, but not H₆HepK, autophosphorylates with [-³²P]ATP. ADP, specifically, elicits dephosphorylation of phosphorylated H₆'HepK. The phosphoryl group of H₆'HepK is transferred rapidly and efficiently to both H₆DevR and H₆DevR_A but not to His-tagged OmpR, whose cognate sensor kinase is EnvZ. Sequence comparisons, the results of site-specific mutagenesis, and tests of chemical stability support identification of HepK-His³⁴⁸ and DevR-Asp⁵³ as the phosphorylated residues. The mutation HepK-H348A abolishes both in vitro autokinase activity and in vivo functionality of HepK. Heterocysts of both hepK Anabaena and devR_A Anabaena lack an envelope polysaccharide layer and are nonfunctional. Consistent with the normal site of deposition of that polysaccharide, a hepK::gfp transcriptional fusion is expressed principally in proheterocysts. HepK/DevR_A is the first two-component system identified that regulates the biosynthesis of a polysaccharide as part of a patterned differentiation process.

Received for publication, January 17, 2003 , and in revised form, February 28, 2003.

^* This work was supported by United States Department of Energy Grant DOE-FG02-91ER20021 and by National Science Foundation Grants MCB 9723193 and MCB 0090232. 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.

Permanent address: College of Life Sciences, Anhui Normal University, Wuhu, Anhui 241000, The People's Republic of China.

^|| To whom correspondence should be addressed: MSU-DOE Plant Research Laboratory, Michigan State University, E. Lansing, MI 48824. Tel.: 517-353-2049; Fax: 517-353-9168; E-mail: wolk{at}msu.edu.

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