Signal transduction in chemotaxis to oxygen in Escherichia coli and Salmonella typhimurium

Abstract

Pathways previously proposed for sensory transduction in chemotaxis to oxygen (aerotaxis) involved either (i) cytochrome o, the electron transport system, and proton motive force or (ii) enzyme 11Iu'co" and the phosphoenolpyruvate:carbohydrate phosphotransferase system for active transport. This investigation distinguished between these possibilities. Aerotaxis was absent in a cyo cyd strain of Escherichia coli that lacked both cytochrome o and cytochrome d, which are the terminal oxidases for the branched electron transport system in E. coli. Aerotaxis, measured by either a spatial or temporal assay, was normal in E. coli strains that had a cyo+ or cyd+ gene or both. The membrane potential of all oxidase-positive strains was approximately -170 mV in aerated medium at pH 7.5. Behavioral responses to changes in oxygen concentration correlated with changes in proton motive force. Aerotaxis was normal in ptsG and ptsl strains that lack enzyme 11G,ucose and enzyme I, respectively, and are deficient in the phosphotransferase system. A cya strain that is deficient in adenylate cyclase also had normal aerotaxis. We concluded that aerotaxis was mediated by the electron transport system and that either the cytochrome d or the cytochrome o branch of the pathway could mediate aerotaxis.We previously proposed a sequence for the initial sensory transduction events in the chemotactic response to oxygen (aerotaxis) by Salmonella typhimurium and Escherichia coli (14-16, 28, 31, 32). According to that model, oxygen increases the flow of reducing equivalents through the respiratory chain and thereby increases the proton motive force across the cytoplasmic membrane. The change in proton motive force is detected by a hypothetical sensing mechanism that transmits a signal to the flagellar motors.Indirect evidence supports the proposed role of the proton motive force in aerotaxis. The concentration of oxygen which gives a half-maximal behavioral response is similar to the Km for cytochrome o, the terminal oxidase of the respiratory chain in exponentially growing S. typhimurium and E. coli (14; D. J. Laszlo, Ph.D. dissertation, Loma Linda University, Loma Linda, Calif., 1981). Inhibitors of respiration also inhibit aerotaxis (15,16). At a constant partial pressure of oxygen, an artificially produced change in proton motive force can cause a behavioral response in Bacillus subtilis (18,20,21 (approximately 25 ,ul) was placed between a glass microscope slide and a cover slip, one side of which rested on a piece of cover slip. An aerotactic band along the air-suspension interface was observed and recorded with a video recorder. The third method, employing an air-filled capillary, was described previously (16). A temporal assay was also described previ-

Behavior of Rhizobium meliloti in oxygen gradients

“…The 21% oxygen at the frequency of direction changes in response to chemoeffectors. meniscus neither attracted the motile cells as observed for aerDirection changes occur when the direction of swimming is obic species of bacteria [20], nor repelled the cells as observed reoriented during periodic tumbling (E. coli), reversal (Halofor facultative anaerobic and microaerophilic species [7,8].…”

“…Institute of Biochemistry and Physiology of cells with oxygen using a tetraphenylphosphonium (TPP÷)-selective Plants and Microorganisms, Russian Academy of Sciences, Saratov, electrode, as previously described [7]. Cells were made permeable to 410015 Russian Federation.…”

“…The terminal oxidases of the bacterial respiratory pirillum brasilense Sp7 (ATCC 29145) cells were grown and prepared chain are the primary receptors for oxygen but not the for aerotaxis experiments as described previously [8]. transducers of the aerotactic signal [7,8]. A search continues for other membrane-bound molecules that can bind oxygen (or…”

The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior

“…Previous studies of the behavioral responses of E. coli to oxygen (2,44), other terminal electron acceptors (5), redox molecules (electron carriers) (9), and rapidly metabolized carbon sources (electron donors) (10) demonstrated that a signal for each of these behaviors is generated in the electron transport system. Electron transport and proton motive force are tightly coupled, so it is not possible at this time to distinguish which is the signal for bacterial behavior.…”

“…In preliminary experiments, we have isolated and purified the Aer protein and found a noncovalently bound cofactor that comigrates with FAD in the HPLC profiles (unpublished data). The midpoint redox potential of FAD͞FADH 2 is Ϫ220 mV; the redox potential of Aer-bound FAD is likely to be in the range that permits interaction with dehydrogenases (Ϫ300 mV range) and͞or with ubiquinone (ϩ113 mV) and menaquinone (Ϫ74 mV) (9,44,45). As a result, Aer may sense changes in the electron transport between dehydrogenases and quinones.…”