Energy taxis is the dominant behavior in Azospirillum brasilense

Abstract

Energy taxis encompasses aerotaxis, phototaxis, redox taxis, taxis to alternative electron acceptors, and chemotaxis to oxidizable substrates. The signal for this type of behavior is originated within the electron transport system. Energy taxis was demonstrated, as a part of an overall behavior, in several microbial species, but it did not appear as the dominant determinant in any of them. In this study, we show that most behavioral responses proceed through this mechanism in the alpha-proteobacterium Azospirillum brasilense. First, chemotaxis to most chemoeffectors typical of the azospirilla habitat was found to be metabolism dependent and required a functional electron transport system. Second, other energy-related responses, such as aerotaxis, redox taxis, and taxis to alternative electron acceptors, were found in A. brasilense. Finally, a mutant lacking a cytochrome c oxidase of the cbb(3) type was affected in chemotaxis, redox taxis, and aerotaxis. Altogether, the results indicate that behavioral responses to most stimuli in A. brasilense are triggered by changes in the electron transport system.

FIG. 1

Repellent response of A. brasilense Sp7 to myxothiazol in a temporal gradient assay. (A) Examples of paths of individual cells traced for 5 s within 20 s upon addition of a buffer or myxothiazol (2.5 μM). (B) Reversal frequency of free-swimming cells upon addition of myxothiazol followed by addition of an artificial electron donor (ascorbate + TMPD). The dashed line indicates a prestimulus level of reversal frequency. Reversal frequency was determined by computerized motion analysis.

FIG. 2

The cytN mutant is affected in both aerotaxis and chemotaxis. (A) Aerotactic bands formed by the wild type (Sp7) and the cytN mutant (FAJ851) in a glass capillary. Cells were suspended in chemotaxis buffer supplemented with 10 mM malate. Magnification, ×200. (B) Chemotaxis of wild type (Sp7) and the cytN mutant (FAJ851) in a temporal gradient assay. The cells were challenged with 10 mM attractant, and the mean smooth-swimming response times were determined.

FIG. 3

Scheme showing energy metabolism in A. brasilense and the sites of action for attractants and repellents. Attractants are shown in bold; action of metabolic and respiratory inhibitors is shown by dashed arrows.