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Journal of Bacteriology, October 2001, p. 5885-5895, Vol. 183, No. 20
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.20.5885-5895.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

In Vivo Synthesis of the Periplasmic Domain of TonB Inhibits Transport through the FecA and FhuA Iron Siderophore Transporters of Escherichia coli

S. Peter Howard,1,2 Christina Herrmann,1 Chad W. Stratilo,2 and V. Braun1,*

Mikrobiologie II, Universität Tübingen, D-72076 Tübingen, Germany,1 and Department of Biology, University of Regina, Regina, Saskatchewan, Canada S4S 0A22

Received 21 May 2001/Accepted 12 July 2001

The siderophore transport activities of the two outer membrane proteins FhuA and FecA of Escherichia coli require the proton motive force of the cytoplasmic membrane. The energy of the proton motive force is postulated to be transduced to the transport proteins by a protein complex that consists of the TonB, ExbB, and ExbD proteins. In the present study, TonB fragments lacking the cytoplasmic membrane anchor were exported to the periplasm by fusing them to the cleavable signal sequence of FecA. Overexpressed TonB(33-239), TonB(103-239), and TonB(122-239) fragments inhibited transport of ferrichrome by FhuA and of ferric citrate by FecA, transcriptional induction of the fecABCDE transport genes by FecA, infection by phage phi 80, and killing of cells by colicin M via FhuA. Transport of ferrichrome by FhuADelta 5-160 was also inhibited by TonB(33-239), although FhuADelta 5-160 lacks the TonB box which is involved in TonB binding. The results show that TonB fragments as small as the last 118 amino acids of the protein interfere with the function of wild-type TonB, presumably by competing for binding sites at the transporters or by forming mixed dimers with TonB that are nonfunctional. In addition, the interactions that are inhibited by the TonB fragments must include more than the TonB box, since transport through corkless FhuA was also inhibited. Since the periplasmic TonB fragments cannot assume an energized conformation, these in vivo studies also agree with previous cross-linking and in vitro results, suggesting that neither recognition nor binding to loaded siderophore receptors is the energy-requiring step in the TonB-receptor interactions.

* Corresponding author. Mailing address: Mikrobiologie/Membranphysiologie, Universität Tübingen, Auf der Morgenstelle 28, D-72076 Tübingen, Germany. Phone: (49) 7071-2972096. Fax: (49) 7071-295843. E-mail: volkmar.braun{at}mikrobio.uni-tuebingen.de.

Journal of Bacteriology, October 2001, p. 5885-5895, Vol. 183, No. 20
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.20.5885-5895.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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