DOI: 10.1128/jb.185.16.4707-4716.2003. Role of <i>Pseudomonas putida tol-oprL</i> Gene Products in Uptake of Solutes through the Cytoplasmic Membrane

Role of Pseudomonas putida tol-oprL Gene Products in Uptake of Solutes through the Cytoplasmic Membrane

10.1128/jb.185.16.4707-4716.2003

Crossref journal-article

American Society for Microbiology

Journal of Bacteriology (235)

Abstract

ABSTRACT Proteins of the Tol-Pal (Tol-OprL) system play a key role in the maintenance of outer membrane integrity and cell morphology in gram-negative bacteria. Here we describe an additional role for this system in the transport of various carbon sources across the cytoplasmic membrane. Growth of Pseudomonas putida tol-oprL mutant strains in minimal medium with glycerol, fructose, or arginine was impaired, and the growth rate with succinate, proline, or sucrose as the carbon source was lower than the growth rate of the parental strain. Assays with radiolabeled substrates revealed that the rates of uptake of these compounds by mutant cells were lower than the rates of uptake by the wild-type strain. The pattern and amount of outer membrane protein in the P. putida tol-oprL mutants were not changed, suggesting that the transport defect was not in the outer membrane. Consistently, the uptake of radiolabeled glucose and glycerol in spheroplasts was defective in the P. putida tol-oprL mutant strains, suggesting that there was a defect at the cytoplasmic membrane level. Generation of a proton motive force appeared to be unaffected in these mutants. To rule out the possibility that the uptake defect was due to a lack of specific transporter proteins, the PutP symporter was overproduced, but this overproduction did not enhance proline uptake in the tol-oprL mutants. These results suggest that the Tol-OprL system is necessary for appropriate functioning of certain uptake systems at the level of the cytoplasmic membrane.

Bibliography

Llamas, M. A., RodriÌguez-Herva, J. J., Hancock, R. E. W., Bitter, W., Tommassen, J., & Ramos, J. L. (2003). Role of Pseudomonas putida tol-oprL Gene Products in Uptake of Solutes through the Cytoplasmic Membrane. Journal of Bacteriology, 185(16), 4707â4716.

Authors 6

María A. Llamas (first)
José J. Rodríguez-Herva (additional)
Robert E. W. Hancock (additional)
Wilbert Bitter (additional)
Jan Tommassen (additional)
Juan L. Ramos (additional)

References 56 Referenced 61

Dates

Type	When
Created	22 years, 1 month ago (Aug. 1, 2003, 7:08 p.m.)
Deposited	4 years, 1 month ago (July 29, 2021, 2:09 p.m.)
Indexed	3 days, 14 hours ago (Sept. 3, 2025, 6:50 a.m.)
Issued	22 years ago (Aug. 15, 2003)
Published	22 years ago (Aug. 15, 2003)
Published Print	22 years ago (Aug. 15, 2003)

Funders 0

None

BibTeX

@article{Llamas_2003, title={Role of Pseudomonas putida tol-oprL Gene Products in Uptake of Solutes through the Cytoplasmic Membrane}, volume={185}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.185.16.4707-4716.2003}, DOI={10.1128/jb.185.16.4707-4716.2003}, number={16}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Llamas, María A. and Rodríguez-Herva, José J. and Hancock, Robert E. W. and Bitter, Wilbert and Tommassen, Jan and Ramos, Juan L.}, year={2003}, month=aug, pages={4707–4716} }

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      "journal-title": "J. Bioenerg. Biomembr."
    },
    {
      "key": "e_1_3_2_3_2",
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      "year": "2000",
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      "journal-title": "Gene"
    },
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      "year": "2000",
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      "year": "2001",
      "unstructured": "de Cock, H., M. Pasveer, J. Tomassen, and E. Bouveret. 2001. Identification of phospholipids as new components that assist in the in vitro trimerization of a bacterial pore protein. Eur. J. Biochem.268:865-875.",
      "journal-title": "Eur. J. Biochem."
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      "journal-title": "J. Biol. Chem."
    },
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    },
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      "key": "e_1_3_2_23_2",
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      "year": "1995",
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      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_27_2",
      "doi-asserted-by": "publisher",
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      "key": "e_1_3_2_28_2",
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      "first-page": "235",
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      "year": "1986",
      "unstructured": "Lazzaroni, J. C., N. Fognini-Lefebvre, and R. C. Portalier. 1986. Effects of lkyB mutations on the expression ompF, ompC and lamB porin structural genes in Escherichia coli K-12. FEMS Microbiol. Lett.33:235-239.",
      "journal-title": "FEMS Microbiol. Lett."
    },
    {
      "key": "e_1_3_2_30_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/jb.145.3.1351-1358.1981"
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      "key": "e_1_3_2_31_2",
      "doi-asserted-by": "crossref",
      "first-page": "735",
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      "volume": "6",
      "year": "1992",
      "unstructured": "Lazzaroni, J. C., and R. C. Portalier. 1992. The excC gene of Escherichia coli K-12 required for cell envelope integrity encodes the peptidoglycan-associated lipoprotein (PAL). Mol. Microbiol.6:735-742.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_32_2",
      "doi-asserted-by": "crossref",
      "first-page": "5939",
      "DOI": "10.1073/pnas.88.14.5939",
      "volume": "88",
      "year": "1991",
      "unstructured": "Levengood, S. K., W. F. Beyer, Jr., and R. E. Webster. 1991. TolA: a membrane protein involved in colicin uptake contains an extended helical region. Proc. Natl. Acad. Sci. USA88:5939-5943.",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "e_1_3_2_33_2",
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      "journal-title": "Res. Microbiol."
    },
    {
      "key": "e_1_3_2_36_2",
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      "doi-asserted-by": "crossref",
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      "DOI": "10.1042/bj1320141",
      "volume": "132",
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      "unstructured": "Midgley, M., and E. A. Dawes. 1973. The regulation of transport of glucose and methyl \u03b1-glucoside in Pseudomonas aeruginosa.Biochem. J.132:141-154.",
      "journal-title": "Biochem. J."
    },
    {
      "key": "e_1_3_2_38_2",
      "doi-asserted-by": "publisher",
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      "DOI": "10.1111/j.1365-2958.1992.tb01487.x",
      "volume": "6",
      "year": "1992",
      "unstructured": "Nikaido, M. 1992. Porins and specific channels of bacterial outer membranes. Mol. Microbiol.6:435-442.",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "e_1_3_2_40_2",
      "doi-asserted-by": "publisher",
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      "key": "e_1_3_2_42_2",
      "doi-asserted-by": "publisher",
      "DOI": "10.1128/JB.182.3.821-824.2000"
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    },
    {
      "key": "e_1_3_2_45_2",
      "unstructured": "Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y."
    },
    {
      "key": "e_1_3_2_46_2",
      "doi-asserted-by": "publisher",
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      "journal-title": "Microbiology"
    },
    {
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