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Journal of Bacteriology, August 2003, p. 4707-4716, Vol. 185, No. 16
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.16.4707-4716.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

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

María A. Llamas,1,{dagger} José J. Rodríguez-Herva,1,{ddagger} Robert E. W. Hancock,2 Wilbert Bitter,3,{dagger} Jan Tommassen,3 and Juan L. Ramos1*

Department of Biochemistry and Molecular and Cellular Biology of Plants, Estación Experimental del Zaidín, Consejo Superior de Investigaciones Científicas, 18008 Granada, Spain,1 Department of Microbiology and Immunology, The University of British Columbia, Vancouver, British Columbia, Canada,2 Department of Molecular Microbiology and Institute of Biomembranes, University of Utrecht, CH Utrecht, The Netherlands3

Received 14 February 2003/ Accepted 23 May 2003

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.

* Corresponding author. Mailing address: Estación Experimental del Zaidín—CSIC, Profesor Albareda number 1, 18008 Granada, Spain. Phone: 34 958181608. Fax: 34 958135740. E-mail: jlramos{at}eez.csic.es.

{dagger} Present address: Department of Medical Microbiology and Infection Prevention, VU Medical Center Amsterdam, Amsterdam, The Netherlands.

{ddagger} Present address: Department of Molecular Microbiology and Institute of Biomembranes, University of Utrecht, CH Utrecht, The Netherlands.

Journal of Bacteriology, August 2003, p. 4707-4716, Vol. 185, No. 16
0021-9193/03/$08.00+0     DOI: 10.1128/JB.185.16.4707-4716.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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