Mechanisms of phototaxis and aerotaxis in <i>Halobacterium halobium</i>

Bibikov, Sergei I.; Skulachev, Vladimir P.

doi:10.1016/0014-5793(89)80150-4

Cited by 27 publications

(19 citation statements)

References 18 publications

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“…2). It is noteworthy that oxygen respiration and arginine, as well as some other factors providing a bacteriorhodopsin-independent maintenance of high ⌬ H ϩ levels, were all potent suppressors of the attractant effect of light mediated by the proton-pumping function of bacteriorhodopsin (7)(8)(9)(10). Addition of the protonophorous uncoupler carbonyl cyanide 3-chlorophenylhydrazone (CCCP) at a concentration which eliminated the suppression of the photoresponse in the presence of very bright light (7,8) suppressed the sensitivity of the blue light reversal response.…”

Section: Resultsmentioning

confidence: 99%

“…We have shown previously that in addition to the two specific photosensory systems sRI and sRII, H. salinarium has a third photosensory pathway in which photoreception is mediated by the proton-pumping activity of bacteriorhodopsin (7)(8)(9)(10).…”

Section: Discussionmentioning

confidence: 99%

“…This function is related to the proton-translocating activity of bacteriorhodopsin (7-10), and it has been suggested that receptor function is mediated by a device that monitors electrochemical gradient of hydrogen ions across the membrane (⌬ H ϩ) called a protometer (5,6,10,15,35). This supports other data on the photoreceptory function of bacteriorhodopsin which also attributed the effects of bacteriorhodopsin on swimming behavior to a secondary consequence of electrogenic proton pumping on metabolic or signal-transducing pathways rather than to primary sensory signaling such as that mediated by sRI (46).…”

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delta psi-mediated signalling in the bacteriorhodopsin-dependent photoresponse

et al. 1996

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It has been shown previously that the proton-pumping activity of bacteriorhodopsin from Halobacterium salinarium can transmit an attractant signal to the bacterial flagella upon an increase in light intensity over a wide range of wavelengths. Here, we studied the effect of blue light on phototactic responses by the mutant strain Pho81-B4, which lacks both sensory rhodopsins but has the ability to synthesize bacteriorhodopsin. Under conditions in which bacteriorhodopsin was largely accumulated as the M 412 bacteriorhodopsin photocycle intermediate, halobacterial cells responded to blue light as a repellent. This response was pronounced when the membrane electric potential level was high in the presence of arginine, active oxygen consumption, or high-background long-wavelength light intensity but was inhibited by an uncoupler of oxidative phosphorylation (carbonyl cyanide 3-chlorophenylhydrazone) and was inverted in a background of low long-wavelength light intensity. The response to changes in the intensity of blue light under high background light was asymmetric, since removal of blue light did not produce an expected suppression of reversals. Addition of ammonium acetate, which is known to reduce the pH gradient changes across the membrane, did not inhibit the repellent effect of blue light, while the discharge of the membrane electric potential by tetraphenylphosphonium ions inhibited this sensory reaction. We conclude that the primary signal from bacteriorhodopsin to the sensory pathway involves changes in membrane potential.Halobacterium salinarium cells swim by means of bipolar flagellar tufts. Smooth swimming is occasionally interrupted by spontaneous cell reversals which are produced by changes in the direction of flagellar rotation. The frequency of spontaneous reversals varies depending on the culture conditions and the particular strain (2,31,38,40,41).An important behavior of halobacteria is phototaxis, which these bacteria use to find the optimal light conditions for photosynthesis and to avoid the harmful effect of UV light. Changes in light intensity are sensed by retinal-containing proteins which control the direction of flagellar rotation through a system of sensory proteins. Increases in UV or blue light intensity or decreases in red or orange light are interpreted by the cells as unfavorable changes of environmental conditions and cause reversal of swimming direction. Decreases in UVblue or increases in red-orange light suppress reversals. Two specialized photosensory systems have been identified in halobacteria. Sensory rhodopsins I and II (sRI [11,38,39] and sRII [24,37,[42][43][44][45], respectively) serve as receptors for light with maximal absorbance at 578 and 487 nm, respectively. Photoexcitation of sRI generates a long-lived sensory rhodopsin intermediate, S 373 , which triggers an attractant response by the cell (11). At the same time, S 373 operates as a third specialized photoreceptor. While attractant light is detected by the ground form of the sRI molecule, repellent light is detec...

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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delta psi-mediated signalling in the bacteriorhodopsin-dependent photoresponse

et al. 1996

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“…Interestingly, under intense light, bacteriorhodopsin also mediates a phototactic response by an unknown mechanism based on changes in the proton motive force (11,12). H. salinarium cells are aerotactic (41), and it has been proposed that ApffH-reception is also the mechanism for aerotaxis in H. salinarium (42). Aerotaxis is methylation-dependent in the Archaeon H. salinarium (43).…”

Section: Identification Of Transducermentioning

confidence: 99%

Signal transduction in the archaeon Halobacterium salinarium is processed through three subfamilies of 13 soluble and membrane-bound transducer proteins.

Zhang

Brooun

McCandless

et al. 1996

Proc. Natl. Acad. Sci. U.S.A.

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Eubacterial transducers are transmembrane, methyl-accepting proteins central to chemotaxis systems and share common structural features. We identified a large family of transducer proteins in the Archaeon Halobacterium salinarium using a site-specific multiple antigenic peptide antibody raised against 23 amino acids, representing the highest homology region of eubacterial transducers. This immunological observation was confirmed by isolating 13 methyl-accepting taxis genes using a 27-mer oligonucleotide probe, corresponding to conserved regions between the eubacterial and first halobacterial phototaxis transducer gene htrI. On the basis of the comparison of the predicted structural domains of these transducers, we propose that at least three distinct subfamilies of transducers exist in the Archaeon H. salinarium: (i) (SRI and SRII), mediate "color vision" (4). Both are retinalcontaining proteins distinct from the retinal-based, lightdriven ion pumps bacteriorhodopsin and halorhodopsin (5-7). SRI is the photoreceptor for green-red and UV light stimuli, and SRII is the photoreceptor for blue light (7-10). Even in the absence of the dedicated sensory rhodopsins, proton pumping by bacteriorhodopsin generates phototaxis responses, probably because of effects on membrane potential or proton motive force (11,12).We and others (13-15) identified a family of methylaccepting taxis proteins with (apparent) molecular masses between 90 and 135 kDa as components of both the photosensory and chemosensory systems in H. salinarium. These proteins are altered in levels of methylation by positive and negative chemostimuli (13) To identify and isolate other transducers involved in halobacterial signal transduction, we used immunological, genetic, and biochemical approaches. This paper describes for the first time the identification and isolation of all the methylaccepting taxis genes, and the localization of their products in the Archaeon H. salinarium.

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“…Aerotaxis in the aerobe Bacillus subtilis (41), in the facultative anaerobes Escherichia coli, Salmonella typhimurium (1,34,36), and Halobacterium salinarium (7,29), and in the anaerobe Desulfovibrio vulgaris (22) has been extensively investigated. At least one motile bacterial species, Rhizobium meliloti, does not have a true chemotactic response to oxygen and responds to oxygen only by chemokinesis (45).…”

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Oxygen taxis and proton motive force in Azospirillum brasilense

et al. 1996

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The microaerophilic nitrogen-fixing bacterium Azospirillum brasilense formed a sharply defined band in a spatial gradient of oxygen. As a result of aerotaxis, the bacteria were attracted to a specific low concentration of oxygen (3 to 5 M). Bacteria swimming away from the aerotactic band were repelled by the higher or lower concentration of oxygen that they encountered and returned to the band. This behavior was confirmed by using temporal gradients of oxygen. The cellular energy level in A. brasilense, monitored by measuring the proton motive force, was maximal at 3 to 5 M oxygen. The proton motive force was lower at oxygen concentrations that were higher or lower than the preferred oxygen concentration. Bacteria swimming toward the aerotactic band would experience an increase in the proton motive force, and bacteria swimming away from the band would experience a decrease in the proton motive force. It is proposed that the change in the proton motive force is the signal that regulates positive and negative aerotaxis. The preferred oxygen concentration for aerotaxis was similar to the preferred oxygen concentration for nitrogen fixation. Aerotaxis is an important adaptive behavioral response that can guide these free-living diazotrophs to the optimal niche for nitrogen fixation in the rhizosphere.Aerotaxis (chemotaxis to oxygen) enables bacteria to find concentrations of dissolved oxygen that are favorable for their metabolic lifestyle (reviewed in references 39 and 40). Aerotaxis was the first behavioral response reported for microorganisms: in 1881, Engelmann described accumulation of Bacterium termo around plant cells that were producing oxygen (10). Among the bacteria described by Engelmann, the most sensitive to oxygen was Spirillum tenue, which accumulated at a low oxygen concentration (11). In 1893, Beijerinck described the formation of bacterial "Atmungsfiguren" around the source of oxygen. The bacteria, most likely spirilla, formed a band at some distance from the oxygen source; the band descended if air was replaced by oxygen or ascended if air was replaced by hydrogen (4). In 1901, Jennings and Crosby investigated the aggregation of Spirillum species in the region of illuminated algae that were evolving oxygen. The bacteria that were distant from the algae swam randomly. However, the cells became trapped if they entered a zone around the algae that had an optimal concentration of oxygen. Whenever the bacteria reached the edge of the zone, the direction of their movement was reversed (20). This aerotactic response, originally termed phobo-chemotaxis (33), resulted in the accumulation of bacteria in the zone of optimal oxygen concentration.Formation of aerotactic bands is a characteristic of motile bacterial species. Aerotaxis in the aerobe Bacillus subtilis (41), in the facultative anaerobes Escherichia coli, Salmonella typhimurium (1, 34, 36), and Halobacterium salinarium (7,29), and in the anaerobe Desulfovibrio vulgaris (22) has been extensively investigated. At least one motile bacterial species, R...

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Mechanisms of phototaxis and aerotaxis in Halobacterium halobium

Cited by 27 publications

References 18 publications

delta psi-mediated signalling in the bacteriorhodopsin-dependent photoresponse

delta psi-mediated signalling in the bacteriorhodopsin-dependent photoresponse

Signal transduction in the archaeon Halobacterium salinarium is processed through three subfamilies of 13 soluble and membrane-bound transducer proteins.

Oxygen taxis and proton motive force in Azospirillum brasilense

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