Three cdg Operons Control Cellular Turnover of Cyclic Di-GMP in Acetobacter xylinum: Genetic Organization and Occurrence of Conserved Domains in Isoenzymes

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Journal of Bacteriology, September 1998, p. 4416-4425, Vol. 180, No. 17
0021-9193/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Three cdg Operons Control Cellular Turnover of Cyclic Di-GMP in Acetobacter xylinum: Genetic Organization and Occurrence of Conserved Domains in Isoenzymes

Rony Tal,¹^, Hing C. Wong,¹^, Roger Calhoon,¹ David Gelfand,¹^, Anna Lisa Fear,¹^,^§ Gail Volman,² Raphael Mayer,²^, Peter Ross,² Dorit Amikam,² Haim Weinhouse,² Avital Cohen,² Shai Sapir,² Patricia Ohana,² and Moshe Benziman²^,^*

Cetus Corporation, Emeryville, California 94608,¹ and Department of Biological Chemistry, The Institute of Life Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel²

Received 13 April 1998/Accepted 18 June 1998

Cyclic di-GMP (c-di-GMP) is the specific nucleotide regulator of $beta$ -1,4-glucan (cellulose) synthase in Acetobacter xylinum.The enzymes controlling turnover of c-di-GMP are diguanylate cyclase(DGC), which catalyzes its formation, and phosphodiesterase A(PDEA), which catalyzes its degradation. Following biochemicalpurification of DGC and PDEA, genes encoding isoforms of theseenzymes have been isolated and found to be located on three distinctyet highly homologous operons for cyclic diguanylate, cdg1, cdg2,and cdg3. Within each cdg operon, a pdeA gene lies upstream ofa dgc gene. cdg1 contains two additional flanking genes, cdg1aand cdg1d. cdg1a encodes a putative transcriptional activator,similar to AadR of Rhodopseudomonas palustris and FixK proteinsof rhizobia. The deduced DGC and PDEA proteins have an identicalmotif structure of two lengthy domains in their C-terminal regions.These domains are also present in numerous bacterial proteinsof undefined function. The N termini of the DGC and PDEA deducedproteins contain putative oxygen-sensing domains, based on similarityto domains on bacterial NifL and FixL proteins, respectively.Genetic disruption analyses demonstrated a physiological hierarchyamong the cdg operons, such that cdg1 contributes 80% of cellularDGC and PDEA activities and cdg2 and cdg3 contribute 15 and 5%,respectively. Disruption of dgc genes markedly reduced in vivocellulose production, demonstrating that c-di-GMP controls thisprocess.

^* Corresponding author. Mailing address: Department of Biological Chemistry, The Institute of Life Sciences, The Hebrew Universityof Jerusalem, Jerusalem 91904, Israel. Phone: 972-2-658 5430.Fax: 972-2-658 6448. E-mail: benziman{at}vms.huji.ac.il.

Present address: Sunol Molecular Corporation, Miami, FL 33172.

Present address: Roche Molecular Systems, Emeryville, CA 94608.

^§ Present address: Chiron Corporation, Emeryville, CA 94608.

Present address: Department of Agricultural Botany and the Otto Warburg Center for Biotechnology in Agriculture, Faculty ofAgriculture, The Hebrew University of Jerusalem, Rehovot 76100,Israel.

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