Cloning and Molecular Analysis of a Mannitol Operon of Phosphoenolpyruvate-dependent Phosphotransferase (PTS) Type from Vibrio Cholerae O395

Overview

Journal Arch Microbiol

Specialty Microbiology

Date 2010 Dec 25

PMID 21184218

Citations 17

Authors

Sanath Kumar

Kenneth P Smith

Jody L Floyd

Manuel F Varela

Affiliations

Soon will be listed here.

Abstract

A putative mannitol operon of the phosphoenolpyruvate phosphotransferase (PTS) type was cloned from Vibrio cholerae O395, and its activity was studied in Escherichia coli. The 3.9-kb operon comprising three genes is organized as mtlADR. Based on the sequence analysis, these were identified as genes encoding a putative mannitol-specific enzyme IICBA (EII(Mtl)) component (MtlA), a mannitol-1-phosphate dehydrogenase (MtlD), and a mannitol operon repressor (MtlR). The transport of [(3)H]mannitol by the cloned mannitol operon in E. coli was 13.8 ± 1.4 nmol/min/mg protein. The insertional inactivation of EII(Mtl) abolished mannitol and sorbitol transport in V. cholerae O395. Comparison of the mannitol utilization apparatus of V. cholerae with those of Gram-negative and Gram-positive bacteria suggests highly conserved nature of the system. MtlA and MtlD exhibit 75% similarity with corresponding sequences of E. coli mannitol operon genes, while MtlR has 63% similarity with MtlR of E. coli. The cloning of V. cholerae mannitol utilization system in an E. coli background will help in elucidating the functional properties of this operon.

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References

Hengstenberg W, Kohlbrecher D, Witt E, Kruse R, Christiansen I, Peters D . Structure and function of proteins of the phosphotransferase system and of 6-phospho-beta-glycosidases in gram-positive bacteria. FEMS Microbiol Rev. 1993; 12(1-3):149-63. DOI: 10.1111/j.1574-6976.1993.tb00016.x. View

Lee C, Saier Jr M . Mannitol-specific enzyme II of the bacterial phosphotransferase system. III. The nucleotide sequence of the permease gene. J Biol Chem. 1983; 258(17):10761-7. View

Akagawa E, Kurita K, Sugawara T, Nakamura K, Kasahara Y, Ogasawara N . Determination of a 17,484 bp nucleotide sequence around the 39 degrees region of the Bacillus subtilis chromosome and similarity analysis of the products of putative ORFs. Microbiology (Reading). 1995; 141 ( Pt 12):3241-5. DOI: 10.1099/13500872-141-12-3241. View

Saier Jr M, Grenier F, Lee C, Waygood E . Evidence for the evolutionary relatedness of the proteins of the bacterial phosphoenolpyruvate:sugar phosphotransferase system. J Cell Biochem. 1985; 27(1):43-56. DOI: 10.1002/jcb.240270106. View

Davanloo P, Rosenberg A, Dunn J, Studier F . Cloning and expression of the gene for bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A. 1984; 81(7):2035-9. PMC: 345431. DOI: 10.1073/pnas.81.7.2035. View

Wang H, Yan M, Zhao Y, Kan B . [Transcriptional repressor gene--mtlR of mannitol PTS operon in Vibrio cholerae]. Wei Sheng Wu Xue Bao. 2007; 47(3):522-5. View

Pas H, Robillard G . Bacterial phosphoenolpyruvate-dependent phosphotransferase system: mannitol-specific EII contains two phosphoryl binding sites per monomer and one high-affinity mannitol binding site per dimer. Biochemistry. 1988; 27(15):5520-5. DOI: 10.1021/bi00415a020. View

Fischer R, Eisermann R, Reiche B, Hengstenberg W . Cloning, sequencing and overexpression of the mannitol-specific enzyme-III-encoding gene of Staphylococcus carnosus. Gene. 1989; 82(2):249-57. DOI: 10.1016/0378-1119(89)90050-4. View

Stoop J, Mooibroek H . Cloning and characterization of NADP-mannitol dehydrogenase cDNA from the button mushroom, Agaricus bisporus, and its expression in response to NaCl stress. Appl Environ Microbiol. 1998; 64(12):4689-96. PMC: 90910. DOI: 10.1128/AEM.64.12.4689-4696.1998. View

10.

Henstra S, Tolner B, ten Hoeve Duurkens R, Konings W, Robillard G . Cloning, expression, and isolation of the mannitol transport protein from the thermophilic bacterium Bacillus stearothermophilus. J Bacteriol. 1996; 178(19):5586-91. PMC: 178395. DOI: 10.1128/jb.178.19.5586-5591.1996. View

11.

Fischer R, Hengstenberg W . Mannitol-specific enzyme II of the phosphoenolpyruvate-dependent phosphotransferase system of Staphylococcus carnosus. Sequence and expression in Escherichia coli and structural comparison with the enzyme IImannitol of Escherichia coli. Eur J Biochem. 1992; 204(3):963-9. DOI: 10.1111/j.1432-1033.1992.tb16717.x. View

12.

Altschul S, Madden T, Schaffer A, Zhang J, Zhang Z, Miller W . Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997; 25(17):3389-402. PMC: 146917. DOI: 10.1093/nar/25.17.3389. View

13.

Lee C, Jacobson G, Saier Jr M . Plasmid-directed synthesis of enzymes required for D-mannitol transport and utilization in Escherichia coli. Proc Natl Acad Sci U S A. 1981; 78(12):7336-40. PMC: 349261. DOI: 10.1073/pnas.78.12.7336. View

14.

Thompson J, Higgins D, Gibson T . CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994; 22(22):4673-80. PMC: 308517. DOI: 10.1093/nar/22.22.4673. View

15.

Postma P, Lengeler J . Phosphoenolpyruvate:carbohydrate phosphotransferase system of bacteria. Microbiol Rev. 1985; 49(3):232-69. PMC: 373035. DOI: 10.1128/mr.49.3.232-269.1985. View

16.

Behrens S, Mitchell W, Bahl H . Molecular analysis of the mannitol operon of Clostridium acetobutylicum encoding a phosphotransferase system and a putative PTS-modulated regulator. Microbiology (Reading). 2001; 147(Pt 1):75-86. DOI: 10.1099/00221287-147-1-75. View

17.

Saier Jr M . Bacterial phosphoenolpyruvate: sugar phosphotransferase systems: structural, functional, and evolutionary interrelationships. Bacteriol Rev. 1977; 41(4):856-71. PMC: 414030. DOI: 10.1128/br.41.4.856-871.1977. View

18.

Lengeler J, Jahreis K, Wehmeier U . Enzymes II of the phospho enol pyruvate-dependent phosphotransferase systems: their structure and function in carbohydrate transport. Biochim Biophys Acta. 1994; 1188(1-2):1-28. DOI: 10.1016/0005-2728(94)90017-5. View

19.

Meadow N, REVUELTA R, Chen V, Colwell R, Roseman S . Phosphoenolpyruvate:glycose phosphotransferase system in species of Vibrio, a widely distributed marine bacterial genus. J Bacteriol. 1987; 169(11):4893-900. PMC: 213882. DOI: 10.1128/jb.169.11.4893-4900.1987. View

20.

WOLFF J, Kaplan N . D-Mannitol 1-phosphate dehydrogenase from Escherichia coli. J Biol Chem. 1956; 218(2):849-69. View