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Interactions of the Energy Transducer TonB with Noncognate Energy-Harvesting Complexes

Kerry K. Brinkman and Ray A. Larsen^*

Department of Biological Sciences, Bowling Green State University, Bowling Green, Ohio 43403

Received 11 July 2007/ Accepted 15 October 2007

The TonB and TolA proteins are energy transducers that couple the ion electrochemical potential of the cytoplasmic membrane to support energy-dependent processes at the outer membrane of the gram-negative envelope. The transfer of energy to these transducers is facilitated by energy-harvesting complexes, which are heteromultimers of cytoplasmic membrane proteins with homologies to proton pump proteins of the flagellar motor. Although the cognate energy-harvesting complex best services each transducer, components of the complexes (for TonB, ExbB and ExbD; for TolA, TolQ and TolR) are sufficiently similar that each complex can imperfectly replace the other. Previous investigations of this molecular cross talk considered energy-harvesting complex components expressed from multicopy plasmids in strains in which the corresponding genes were interrupted by insertions, partially absent due to polarity, or missing due to a larger deletion. These questions were reexamined here using strains in which individual genes were removed by precise deletions and, where possible, components were expressed from single-copy genes with native promoters. By more closely approximating natural stoichiometries between components, this study provided insight into the roles of energy-harvesting complexes in both the energization and the stabilization of TonB. Further, the data suggest a distinct role for ExbD in the TonB energy transduction cycle.

Published ahead of print on 26 October 2007.

Present address: Department of Microbiology, University of Pennsylvania School of Medicine, Philadelphia, PA 19104.