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Journal of Bacteriology, July 2004, p. 4075-4084, Vol. 186, No. 13
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.13.4075-4084.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

A Gene from the Mesophilic Bacterium Dehalococcoides ethenogenes Encodes a Novel Mannosylglycerate Synthase

Nuno Empadinhas,1 Luciana Albuquerque,1 Joana Costa,1 Stephen H. Zinder,2 Manuel A. S. Santos,3 Helena Santos,4 and Milton S. da Costa1*

Departamento de Bioquímica, Centro de Neurociências e Biologia Celular, and Departamento de Zoologia, Universidade de Coimbra, 3004-517 Coimbra,1 Centro de Biologia Celular, Departamento de Biologia, Universidade de Aveiro, 3810-193 Aveiro,3 Instituto de Tecnologia Química e Biológica, Universidade Nova de Lisboa, 2780-156 Oeiras, Portugal,4 Department of Microbiology, Cornell University, Ithaca, New York 148532

Received 27 January 2004/ Accepted 22 March 2004

Mannosylglycerate (MG) is a common compatible solute found in thermophilic and hyperthermophilic prokaryotes. In this study we characterized a mesophilic and bifunctional mannosylglycerate synthase (MGSD) encoded in the genome of the bacterium Dehalococcoides ethenogenes. mgsD encodes two domains with extensive homology to mannosyl-3-phosphoglycerate synthase (MPGS, EC 2.4.1.217) and to mannosyl-3-phosphoglycerate phosphatase (MPGP, EC 3.1.3.70), which catalyze the consecutive synthesis and dephosphorylation of mannosyl-3-phosphoglycerate to yield MG in Pyrococcus horikoshii, Thermus thermophilus, and Rhodothermus marinus. The bifunctional MGSD was overproduced in Escherichia coli, and we confirmed the combined MPGS and MPGP activities of the recombinant enzyme. The optimum activity of the enzyme was at 50°C. To examine the properties of each catalytic domain of MGSD, we expressed them separately in E. coli. The monofunctional MPGS was unstable, while the MPGP was stable and was characterized. Dehalococcoides ethenogenes cannot be grown sufficiently to identify intracellular compatible solutes, and E. coli harboring MGSD did not accumulate MG. However, Saccharomyces cerevisiae expressing mgsD accumulated MG, confirming that this gene product can synthesize this compatible solute and arguing for a role in osmotic adjustment in the natural host. We did not detect MGSD activity in cell extracts of S. cerevisiae. Here we describe the first gene and enzyme for the synthesis of MG from a mesophilic microorganism and discuss the possible evolution of this bifunctional MGSD by lateral gene transfer from thermophilic and hyperthermophilic organisms.

* Corresponding author. Mailing address: Centro de Neurociências e Biologia Celular, Departamento de Zoologia, Universidade de Coimbra, 3004-517 Coimbra, Portugal. Phone: 351-23982402. Fax: 351-239826798. E-mail: milton{at}ci.uc.pt.

Journal of Bacteriology, July 2004, p. 4075-4084, Vol. 186, No. 13
0021-9193/04/$08.00+0     DOI: 10.1128/JB.186.13.4075-4084.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Fernandes, C., Empadinhas, N., da Costa, M. S. (2007). Single-Step Pathway for Synthesis of Glucosylglycerate in Persephonella marina. J. Bacteriol. 189: 4014-4019 [Abstract] [Full Text]  
  • Costa, J., Empadinhas, N., da Costa, M. S. (2007). Glucosylglycerate Biosynthesis in the Deepest Lineage of the Bacteria: Characterization of the Thermophilic Proteins GpgS and GpgP from Persephonella marina. J. Bacteriol. 189: 1648-1654 [Abstract] [Full Text]  
  • Costa, J., Empadinhas, N., Goncalves, L., Lamosa, P., Santos, H., da Costa, M. S. (2006). Characterization of the Biosynthetic Pathway of Glucosylglycerate in the Archaeon Methanococcoides burtonii. J. Bacteriol. 188: 1022-1030 [Abstract] [Full Text]  
  • Neves, C., da Costa, M. S., Santos, H. (2005). Compatible Solutes of the Hyperthermophile Palaeococcus ferrophilus: Osmoadaptation and Thermoadaptation in the Order Thermococcales. Appl. Environ. Microbiol. 71: 8091-8098 [Abstract] [Full Text]  


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