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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,dagger Hing C. Wong,1,dagger Roger Calhoon,1 David Gelfand,1,Dagger Anna Lisa Fear,1,§ Gail Volman,2 Raphael Mayer,2,parallel 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 biochemical purification of DGC and PDEA, genes encoding isoforms of these enzymes have been isolated and found to be located on three distinct yet highly homologous operons for cyclic diguanylate, cdg1, cdg2, and cdg3. Within each cdg operon, a pdeA gene lies upstream of a dgc gene. cdg1 contains two additional flanking genes, cdg1a and cdg1d. cdg1a encodes a putative transcriptional activator, similar to AadR of Rhodopseudomonas palustris and FixK proteins of rhizobia. The deduced DGC and PDEA proteins have an identical motif structure of two lengthy domains in their C-terminal regions. These domains are also present in numerous bacterial proteins of undefined function. The N termini of the DGC and PDEA deduced proteins contain putative oxygen-sensing domains, based on similarity to domains on bacterial NifL and FixL proteins, respectively. Genetic disruption analyses demonstrated a physiological hierarchy among the cdg operons, such that cdg1 contributes 80% of cellular DGC and PDEA activities and cdg2 and cdg3 contribute 15 and 5%, respectively. Disruption of dgc genes markedly reduced in vivo cellulose production, demonstrating that c-di-GMP controls this process.

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

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

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

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

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

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.


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