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PMID: 9457875 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Archaeal binding protein-dependent ABC transporter: molecular and biochemical analysis of the trehalose/maltose transport system of the hyperthermophilic archaeon Thermococcus litoralis.

Journal of bacteriology ·Vol. 180 ·No. 3 ·1998-02-00 ·Pages 680-9

Horlacher R, Xavier KB, Santos H, DiRuggiero J, Kossmann M, Boos W

Abstract

We report the cloning and sequencing of a gene cluster encoding a maltose/trehalose transport system of the hyperthermophilic archaeon Thermococcus litoralis that is homologous to the malEFG cluster encoding the Escherichia coli maltose transport system. The deduced amino acid sequence of the malE product, the trehalose/maltose-binding protein (TMBP), shows at its N terminus a signal sequence typical for bacterial secreted proteins containing a glyceride lipid modification at the N-terminal cysteine. The T. litoralis malE gene was expressed in E. coli under control of an inducible promoter with and without its natural signal sequence. In addition, in one construct the endogenous signal sequence was replaced by the E. coli MalE signal sequence. The secreted, soluble recombinant protein was analyzed for its binding activity towards trehalose and maltose. The protein bound both sugars at 85 degrees C with a Kd of 0.16 microM. Antibodies raised against the recombinant soluble TMBP recognized the detergent-soluble TMBP isolated from T. litoralis membranes as well as the products from all other DNA constructs expressed in E. coli. Transmembrane segments 1 and 2 as well as the N-terminal portion of the large periplasmic loop of the E. coli MalF protein are missing in the T. litoralis MalF. MalG is homologous throughout the entire sequence, including the six transmembrane segments. The conserved EAA loop is present in both proteins. The strong homology found between the components of this archaeal transport system and the bacterial systems is evidence for the evolutionary conservation of the binding protein-dependent ABC transport systems in these two phylogenetic branches.

MeSH Terms
ATP-Binding Cassette Transporters/biosynthesis,genetics,isolation & purification,metabolism Amino Acid Sequence Archaeal Proteins/biosynthesis,genetics,isolation & purification,metabolism Bacterial Proteins/genetics,metabolism Base Sequence Carrier Proteins/biosynthesis,genetics,isolation & purification,metabolism Cell Membrane/metabolism Cloning, Molecular DNA, Archaeal Escherichia coli/metabolism Escherichia coli Proteins Gene Expression Maltose/metabolism Maltose-Binding Proteins Membrane Proteins/biosynthesis,genetics,isolation & purification,metabolism Molecular Sequence Data Monosaccharide Transport Proteins Operon Periplasmic Binding Proteins Sequence Homology, Amino Acid Thermococcus/genetics,metabolism Trehalose/metabolism
Chemicals
ATP-Binding Cassette Transporters Archaeal Proteins Bacterial Proteins Carrier Proteins DNA, Archaeal Escherichia coli Proteins MalE protein, E coli MalG protein, E coli Maltose-Binding Proteins Membrane Proteins Monosaccharide Transport Proteins Periplasmic Binding Proteins maltose transport system, E coli Maltose Trehalose
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Horlacher R
Department of Biology, University of Konstanz, Germany.
Xavier K B
Santos H
DiRuggiero J
Kossmann M
Boos W
References (42)
42 references, click to expand
  1. Analysis of the topology of a membrane protein by using a minimum number of alkaline phosphatase fusions.
    J Bacteriol. 1993 Jan;175(2):553-6 PMID: 8419303
  2. Biochemical identification of a lipoprotein with maltose-binding activity in the thermoacidophilic Gram-positive bacterium Alicyclobacillus acidocaldarius.
    Res Microbiol. 1996 Nov-Dec;147(9):733-7 PMID: 9296107
  3. A signal sequence is not required for protein export in prlA mutants of Escherichia coli.
    EMBO J. 1993 Mar;12(3):879-88 PMID: 8458344
  4. Structure of the maltodextrin-uptake locus of Streptococcus pneumoniae. Correlation to the Escherichia coli maltose regulon.
    J Mol Biol. 1993 Apr 5;230(3):800-11 PMID: 8478935
  5. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria.
    Microbiol Rev. 1993 Jun;57(2):320-46 PMID: 8336670
  6. Trehalose-6-phosphate hydrolase of Escherichia coli.
    J Bacteriol. 1994 Sep;176(18):5654-64 PMID: 8083158
  7. Bacterial binding protein-dependent permeases: characterization of distinctive signatures for functionally related integral cytoplasmic membrane proteins.
    Mol Microbiol. 1994 Jun;12(6):993-1004 PMID: 7934906
  8. Molecular analysis of treB encoding the Escherichia coli enzyme II specific for trehalose.
    J Bacteriol. 1995 Jul;177(14):4043-52 PMID: 7608078
  9. MalY of Escherichia coli is an enzyme with the activity of a beta C-S lyase (cystathionase).
    J Bacteriol. 1995 Sep;177(17):5035-9 PMID: 7665481
  10. The inhibition of maltose transport by the unliganded form of the maltose-binding protein of Escherichia coli: experimental findings and mathematical treatment.
    J Theor Biol. 1995 Nov 21;177(2):171-9 PMID: 8558904
  11. Molecular analysis of the amy gene locus of Thermoanaerobacterium thermosulfurigenes EM1 encoding starch-degrading enzymes and a binding protein-dependent maltose transport system.
    J Bacteriol. 1996 Feb;178(4):1039-46 PMID: 8576036
  12. Hyperthermostable surface layer protein tetrabrachion from the archaebacterium Staphylothermus marinus: evidence for the presence of a right-handed coiled coil derived from the primary structure.
    J Mol Biol. 1996 Apr 19;257(5):1031-41 PMID: 8632466
  13. High-affinity maltose/trehalose transport system in the hyperthermophilic archaeon Thermococcus litoralis.
    J Bacteriol. 1996 Aug;178(16):4773-7 PMID: 8759837
  14. Crystal structures of various maltooligosaccharides bound to maltoporin reveal a specific sugar translocation pathway.
    Structure. 1996 Feb 15;4(2):127-34 PMID: 8805519
  15. Improved method for the preparative synthesis of labeled trehalose of high specific activity by Escherichia coli.
    Appl Environ Microbiol. 1996 Oct;62(10):3861-3 PMID: 8837441
  16. Targeting of signal sequenceless proteins for export in Escherichia coli with altered protein translocase.
    EMBO J. 1996 Oct 1;15(19):5209-17 PMID: 8895566
  17. The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts.
    J Biol Chem. 1965 Sep;240(9):3685-92 PMID: 4284300
  18. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  19. On the significance of the retention of ligand by protein.
    Proc Natl Acad Sci U S A. 1975 Jun;72(6):2120-4 PMID: 1094454
  20. Purification and properties of the sn-glycerol 3-phosphate-binding protein of Escherichia coli.
    J Biol Chem. 1979 Nov 10;254(21):10931-5 PMID: 387762
  21. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  22. Identification of a cytoplasmic membrane-associated component of the maltose transport system of Escherichia coli.
    J Biol Chem. 1980 Sep 25;255(18):8366-9 PMID: 6997295
  23. Isolation of viral IgY antibodies from yolks of immunized hens.
    Immunol Commun. 1980;9(5):475-93 PMID: 7429529
  24. Identification of the malK gene product. A peripheral membrane component of the Escherichia coli maltose transport system.
    J Biol Chem. 1981 Jan 25;256(2):560-2 PMID: 6778869
  25. A comprehensive set of sequence analysis programs for the VAX.
    Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387-95 PMID: 6546423
  26. Sequences of the malE gene and of its product, the maltose-binding protein of Escherichia coli K12.
    J Biol Chem. 1984 Aug 25;259(16):10606-13 PMID: 6088507
  27. The nucleotide sequence of the gene for malF protein, an inner membrane component of the maltose transport system of Escherichia coli. Repeated DNA sequences are found in the malE-malF intercistronic region.
    J Biol Chem. 1984 Sep 10;259(17):10896-903 PMID: 6088520
  28. Inducible expression vectors incorporating the Escherichia coli atpE translational initiation region.
    Gene. 1987;52(2-3):279-83 PMID: 3038690
  29. Determinants of membrane protein topology.
    Proc Natl Acad Sci U S A. 1987 Dec;84(23):8525-9 PMID: 3317413
  30. Evidence for high affinity binding-protein dependent transport systems in gram-positive bacteria and in Mycoplasma.
    EMBO J. 1988 Dec 1;7(12):3971-4 PMID: 3208757
  31. Nucleotide sequence of the ugp genes of Escherichia coli K-12: homology to the maltose system.
    Mol Microbiol. 1988 Nov;2(6):767-75 PMID: 3062310
  32. Comparison of sequences from the malB regions of Salmonella typhimurium and Enterobacter aerogenes with Escherichia coli K12: a potential new regulatory site in the interoperonic region.
    Mol Gen Genet. 1989 Aug;218(2):199-207 PMID: 2674653
  33. Genetic analysis of membrane protein topology by a sandwich gene fusion approach.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7574-8 PMID: 2170984
  34. Construction and characterization of Escherichia coli strains deficient in multiple secreted proteases: protease III degrades high-molecular-weight substrates in vivo.
    J Bacteriol. 1991 Apr;173(8):2696-703 PMID: 2013581
  35. Control regions of an archaeal gene. A TATA box and an initiator element promote cell-free transcription of the tRNA(Val) gene of Methanococcus vannielii.
    J Mol Biol. 1991 Dec 5;222(3):495-508 PMID: 1748992
  36. Atomic interactions in protein-carbohydrate complexes. Tryptophan residues in the periplasmic maltodextrin receptor for active transport and chemotaxis.
    J Mol Biol. 1992 Jul 5;226(1):15-22 PMID: 1619648
  37. Elements of an archaeal promoter defined by mutational analysis.
    Nucleic Acids Res. 1992 Oct 25;20(20):5423-8 PMID: 1279520
  38. Properties and gene structure of the Thermotoga maritima alpha-amylase AmyA, a putative lipoprotein of a hyperthermophilic bacterium.
    J Bacteriol. 1997 Feb;179(3):941-8 PMID: 9006052
  39. The Streptomyces ATP-binding component MsiK assists in cellobiose and maltose transport.
    J Bacteriol. 1997 Mar;179(6):2092-5 PMID: 9068663
  40. Quantitative analysis of binding protein-mediated ABC transport systems.
    J Theor Biol. 1997 May 7;186(1):65-74 PMID: 9176638
  41. Subunit interactions in ABC transporters: a conserved sequence in hydrophobic membrane proteins of periplasmic permeases defines an important site of interaction with the ATPase subunits.
    EMBO J. 1997 Jun 2;16(11):3066-77 PMID: 9214624
  42. Sequence-function relationships in MalG, an inner membrane protein from the maltose transport system in Escherichia coli.
    Mol Microbiol. 1993 Jan;7(1):39-47 PMID: 8437519
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
DOI
10.1128/JB.180.3.680-689.1998
Published
1998-02-00
Pages
680-9
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC106939
Subset
IM
Databases
GENBANK
AF012836
External Links
PubMed source DOI: 10.1128/JB.180.3.680-689.1998 PMC Full Text View journal details
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