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PMID: 9649434 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Overlapping functions of components of a bacterial Sec-independent protein export pathway.

The EMBO journal ·Vol. 17 ·No. 13 ·1998-07-01 ·Pages 3640-50

Sargent F, Bogsch EG, Stanley NR, Wexler M, Robinson C, Berks BC, Palmer T

Abstract

We describe the identification of two Escherichia coli genes required for the export of cofactor-containing periplasmic proteins, synthesized with signal peptides containing a twin arginine motif. Both gene products are homologous to the maize HCF106 protein required for the translocation of a subset of lumenal proteins across the thylakoid membrane. Disruption of either gene affects the export of a range of such proteins, and a complete block is observed when both genes are inactivated. The Sec protein export pathway was unaffected, indicating the involvement of the gene products in a novel export system. The accumulation of active cofactor-containing proteins in the cytoplasm of the mutant strains suggests a role for the gene products in the translocation of folded proteins. One of the two HCF106 homologues is encoded by the first gene of a four cistron operon, tatABCD, and the second by an unlinked gene, tatE. A mutation previously assigned to the hcf106 homologue encoded at the tatABCD locus, mttA, lies instead in the tatB gene.

MeSH Terms
Bacterial Proteins/genetics,physiology Base Sequence Biological Transport Cloning, Molecular Cytoplasm/metabolism DNA, Bacterial Enzyme Activation Escherichia coli/genetics,growth & development,physiology Formate Dehydrogenases/metabolism Genes, Bacterial Hydrogenase/metabolism Membrane Proteins/chemistry Molecular Sequence Data Mutagenesis Oxidoreductases, N-Demethylating/genetics,metabolism Phenotype Plant Proteins Protein Precursors/metabolism Protein Processing, Post-Translational Recombinant Fusion Proteins/metabolism
Chemicals
Bacterial Proteins DNA, Bacterial Hcf106 protein, plant Membrane Proteins Plant Proteins Protein Precursors Recombinant Fusion Proteins Hydrogenase Formate Dehydrogenases Oxidoreductases, N-Demethylating trimethylamine dehydrogenase
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Sargent F
Nitrogen Fixation Laboratory, John Innes Centre, Colney, Norwich NR4 7UH.
Bogsch E G
Stanley N R
Wexler M
Robinson C
Berks B C
Palmer T
References (58)
58 references, click to expand
  1. A novel sec-independent periplasmic protein translocation pathway in Escherichia coli.
    EMBO J. 1998 Jan 2;17(1):101-12 PMID: 9427745
  2. Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid.
    EMBO J. 1995 Aug 15;14(16):3905-14 PMID: 7664731
  3. Cloning and sequencing of a putative Escherichia coli [NiFe] hydrogenase-1 operon containing six open reading frames.
    J Bacteriol. 1990 Apr;172(4):1969-77 PMID: 2180913
  4. Nickel-containing hydrogenase isoenzymes from anaerobically grown Escherichia coli K-12.
    J Bacteriol. 1985 Aug;163(2):454-9 PMID: 3894325
  5. The purification and properties of formate dehydrogenase and nitrate reductase from Escherichia coli.
    J Biol Chem. 1975 Sep 10;250(17):6693-705 PMID: 1099093
  6. Sites and specificity of the reaction of bipyridylium compounds with anaerobic respiratory enzymes of Escherichia coli. Effects of permeability barriers imposed by the cytoplasmic membrane.
    Biochem J. 1977 Apr 15;164(1):199-211 PMID: 328010
  7. The genetic map of the filamentous bacteriophage f1.
    Virology. 1972 Jul;49(1):45-60 PMID: 4556929
  8. Immunization, isolation of immunoglobulins, estimation of antibody titre.
    Scand J Immunol Suppl. 1973;1:161-4 PMID: 4204108
  9. Lack of copper insertion into unprocessed cytoplasmic nitrous oxide reductase generated by an R20D substitution in the arginine consensus motif of the signal peptide.
    Biochim Biophys Acta. 1997 Apr 11;1319(2-3):311-8 PMID: 9131052
  10. The complete genome sequence of Escherichia coli K-12.
    Science. 1997 Sep 5;277(5331):1453-62 PMID: 9278503
  11. Azide-resistant mutants of Escherichia coli alter the SecA protein, an azide-sensitive component of the protein export machinery.
    Proc Natl Acad Sci U S A. 1990 Nov;87(21):8227-31 PMID: 2146683
  12. Site-directed mutagenesis of the hydrogenase signal peptide consensus box prevents export of a beta-lactamase fusion protein.
    J Gen Microbiol. 1992 Oct;138(10):2173-83 PMID: 1479348
  13. A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the delta pH-dependent thylakoidal protein translocase.
    EMBO J. 1995 Jun 15;14(12):2715-22 PMID: 7796800
  14. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes.
    Proc Natl Acad Sci U S A. 1985 Feb;82(4):1074-8 PMID: 3156376
  15. Evidence for a loop mechanism of protein transport by the thylakoid Delta pH pathway.
    FEBS Lett. 1998 Feb 13;423(1):66-70 PMID: 9506843
  16. Signal sequences. The limits of variation.
    J Mol Biol. 1985 Jul 5;184(1):99-105 PMID: 4032478
  17. Sec-independent protein translocation by the maize Hcf106 protein.
    Science. 1997 Nov 21;278(5342):1467-70 PMID: 9367960
  18. Requirement for nickel of the transmembrane translocation of NiFe-hydrogenase 2 in Escherichia coli.
    FEBS Lett. 1996 Aug 26;392(2):81-6 PMID: 8772179
  19. Nucleotide sequence of the dmsABC operon encoding the anaerobic dimethylsulphoxide reductase of Escherichia coli.
    Mol Microbiol. 1988 Nov;2(6):785-95 PMID: 3062312
  20. Identification and characterization of aarF, a locus required for production of ubiquinone in Providencia stuartii and Escherichia coli and for expression of 2'-N-acetyltransferase in P. stuartii.
    J Bacteriol. 1998 Jan;180(1):128-35 PMID: 9422602
  21. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins.
    Cell. 1998 Apr 3;93(1):93-101 PMID: 9546395
  22. 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
  23. New method for generating deletions and gene replacements in Escherichia coli.
    J Bacteriol. 1989 Sep;171(9):4617-22 PMID: 2548993
  24. Analysis of the Import of Carboxyl-Terminal Truncations of the 23-Kilodalton Subunit of the Oxygen-Evolving Complex Suggests That Its Structure Is an Important Determinant for Thylakoid Transport.
    Plant Physiol. 1996 Aug;111(4):1329-1338 PMID: 12226365
  25. Molecular analysis of dimethylsulfoxide reductase: a complex iron-sulfur molybdoenzyme of Escherichia coli.
    Biochim Biophys Acta. 1992 Aug 28;1102(1):1-18 PMID: 1324728
  26. The hyp operon gene products are required for the maturation of catalytically active hydrogenase isoenzymes in Escherichia coli.
    Arch Microbiol. 1992;158(6):444-51 PMID: 1482271
  27. A monomeric, tightly folded stromal intermediate on the delta pH-dependent thylakoidal protein transport pathway.
    J Biol Chem. 1995 Jan 27;270(4):1663-9 PMID: 7829500
  28. Anaerobic regulation of the hydrogenase 1 (hya) operon of Escherichia coli.
    J Bacteriol. 1994 Sep;176(17):5423-8 PMID: 8071220
  29. The hydrogenases and formate dehydrogenases of Escherichia coli.
    Antonie Van Leeuwenhoek. 1994;66(1-3):57-88 PMID: 7747941
  30. Differential expression of hydrogenase isoenzymes in Escherichia coli K-12: evidence for a third isoenzyme.
    J Bacteriol. 1985 Dec;164(3):1324-31 PMID: 3905769
  31. Regulation of the trimethylamine N-oxide (TMAO) reductase in Escherichia coli: analysis of tor::Mud1 operon fusion.
    Mol Gen Genet. 1984;195(1-2):351-5 PMID: 6387391
  32. The complete general secretory pathway in gram-negative bacteria.
    Microbiol Rev. 1993 Mar;57(1):50-108 PMID: 8096622
  33. Identification of a second gene involved in global regulation of fumarate reductase and other nitrate-controlled genes for anaerobic respiration in Escherichia coli.
    J Bacteriol. 1989 Jul;171(7):3810-6 PMID: 2544557
  34. Pathway specificity for a delta pH-dependent precursor thylakoid lumen protein is governed by a 'Sec-avoidance' motif in the transfer peptide and a 'Sec-incompatible' mature protein.
    EMBO J. 1997 Jul 1;16(13):3851-9 PMID: 9233795
  35. Carboxy-terminal processing of the large subunit of [NiFe] hydrogenases.
    FEBS Lett. 1993 Sep 27;331(1-2):91-5 PMID: 8405419
  36. Analysis of the Escherichia coli genome: DNA sequence of the region from 84.5 to 86.5 minutes.
    Science. 1992 Aug 7;257(5071):771-8 PMID: 1379743
  37. Nitrate-inducible formate dehydrogenase in Escherichia coli K-12. I. Nucleotide sequence of the fdnGHI operon and evidence that opal (UGA) encodes selenocysteine.
    J Biol Chem. 1991 Nov 25;266(33):22380-5 PMID: 1834669
  38. Isolation, characterization, and nucleotide sequence of appY, a regulatory gene for growth-phase-dependent gene expression in Escherichia coli.
    J Bacteriol. 1989 Mar;171(3):1683-91 PMID: 2537825
  39. Sequence analysis of an internal 9.72-kb segment from the 30-kb denitrification gene cluster of Pseudomonas stutzeri.
    Biochim Biophys Acta. 1996 Nov 12;1277(1-2):6-12 PMID: 8950369
  40. The inducible trimethylamine-N-oxide reductase of Escherichia coli K12: biochemical and immunological studies.
    Biochim Biophys Acta. 1988 Apr 28;954(1):1-13 PMID: 3282544
  41. Reversible specific concentration of amino acids in Escherichia coli.
    Ann Inst Pasteur (Paris). 1956 Nov;91(5):693-720 PMID: 13395009
  42. Bacterial reduction of trimethylamine oxide.
    Annu Rev Microbiol. 1985;39:131-49 PMID: 3904597
  43. A 12-cistron Escherichia coli operon (hyf) encoding a putative proton-translocating formate hydrogenlyase system.
    Microbiology. 1997 Nov;143 ( Pt 11):3633-47 PMID: 9387241
  44. Common principles of protein translocation across membranes.
    Science. 1996 Mar 15;271(5255):1519-26 PMID: 8599107
  45. Structural genes for nitrate-inducible formate dehydrogenase in Escherichia coli K-12.
    Genetics. 1990 Aug;125(4):691-702 PMID: 2168848
  46. A folded protein can be transported across the chloroplast envelope and thylakoid membranes.
    Mol Biol Cell. 1997 May;8(5):923-34 PMID: 9168475
  47. TMAO anaerobic respiration in Escherichia coli: involvement of the tor operon.
    Mol Microbiol. 1994 Mar;11(6):1169-79 PMID: 8022286
  48. Protein measurement with the Folin phenol reagent.
    J Biol Chem. 1951 Nov;193(1):265-75 PMID: 14907713
  49. Mechanism of assembly of the outer membrane of Salmonella typhimurium. Site of synthesis of lipopolysaccharide.
    J Biol Chem. 1972 Jun 25;247(12):3973-86 PMID: 4624447
  50. Characterisation of a protease from Escherichia coli involved in hydrogenase maturation.
    Eur J Biochem. 1995 Jan 15;227(1-2):545-50 PMID: 7851435
  51. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4530-3 PMID: 159458
  52. Functional and structural role of the cytochrome b subunit of the membrane-bound hydrogenase complex of Alcaligenes eutrophus H16.
    Eur J Biochem. 1997 Aug 15;248(1):179-86 PMID: 9310376
  53. Signal peptides: exquisitely designed transport promoters.
    Mol Microbiol. 1994 Sep;13(5):765-73 PMID: 7815936
  54. The organization of hydrogenase in the cytoplasmic membrane of Escherichia coli.
    Biochem J. 1981 Aug 1;197(2):283-91 PMID: 7034717
  55. Dimethyl sulfoxide reductase activity by anaerobically grown Escherichia coli HB101.
    J Bacteriol. 1985 Jun;162(3):1151-5 PMID: 3888958
  56. RfaH and the ops element, components of a novel system controlling bacterial transcription elongation.
    Mol Microbiol. 1997 Dec;26(5):845-51 PMID: 9426123
  57. Protein import into chloroplasts. The hydrophilic lumenal proteins exhibit unexpected import and sorting specificities in spite of structurally conserved transit peptides.
    J Biol Chem. 1993 Jul 5;268(19):13869-76 PMID: 8314754
  58. A common export pathway for proteins binding complex redox cofactors?
    Mol Microbiol. 1996 Nov;22(3):393-404 PMID: 8939424
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1998-07-01
Pages
3640-50
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1170700
Subset
IM
Databases
GENBANK
AJ005830
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