Negative Phototaxis from Blue Light and the Role of Third Rhodopsinlike Pigment in Halobacterium Cutirubrum

Takahashi, Tetsuo; Watanabe, Masahiko; Kamo, Naoki; Kobatake, Yonosuke

doi:10.1016/s0006-3495(85)83776-0

Cited by 23 publications

(6 citation statements)

References 17 publications

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“…This light intensity is comparable with or lower than the intensities used by other workers (3,11,12,22,23).…”

Section: Methodssupporting

confidence: 70%

“…Complete action spectra are much more easily obtained by monitoring changes in cell density as a function of spatial differences in light intensity and wavelength. We developed the microscopic method described here to obtain action spectra for the phototactic responses of halobacteria, which, until now, have been obtained mainly by observations of single cells (2,3,22,23) or by a very slow macroscopic technique (14). The basic technique was already used by Engelmann, the discoverer of bacterial phototaxis (6), who observed the accumulation of cells in a field of attractant light.…”

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confidence: 99%

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A rapid population method for action spectra applied to Halobacterium halobium

1988

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We have developed a simple and rapid technique for measuring the action spectra for phototaxis of populations of microorganisms and applied it to halobacteria. A microscope with a dark-field condenser was used to illuminate the cell suspension in a sealed chamber with light of wavelength >750 nm; in this region of the spectrum, the halobacteria show no phototactic response. A 150-p.m spot of light from a xenon arc lamp, whose wavelength and intensity can be varied, was projected through the objective lens into the center of the dark field. The objective lens imaged this measuring spot through a 780-nm cut-off filter on an aperture in front of a photomultiplier. The intensity of the scattered 750-nm light, and therefore the photomultiplier current, is proportional to the number of cells in the measuring spot. A third lamp provided background light of variable wavelength and intensity through the dark-field condenser. To minimize secondary effects due to large changes in cell density, we recorded the initial changes in the photomultiplier current over 1 min after the actinic light had been switched on. By plotting the rate of change against wavelength, we obtained action spectra after the proper corrections for changes in light intensity with wavelength were applied and saturation effects were avoided.

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“…This light intensity is comparable with or lower than the intensities used by other workers (3,11,12,22,23).…”

Section: Methodssupporting

confidence: 70%

mentioning

confidence: 99%

A rapid population method for action spectra applied to Halobacterium halobium

1988

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“…BR operates as a light-driven H+ pump (2), HR operates as a chloride pump (5), and SRI (6) and SRII (7,8) the cytoplasm via Asp-96. SRs are present in the same cells in much smaller amounts than BR.…”

Section: Introductionmentioning

confidence: 99%

“…Halobacterium salinarium [formerly Halobacterium halobium (1)] contains four retinal proteins: bacteriorhodopsin (BR) (2,3), halorhodopsin (HR) (4,5), and sensory rhodopsins (SRs) I and II (6,7). BR operates as a light-driven H+ pump (2), HR operates as a chloride pump (5), and SRI (6) and SRII (7,8) are specialized light sensors.…”

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confidence: 99%

Bacteriorhodopsin is involved in halobacterial photoreception.

Bibikov

Grishanin

Kaulen

et al. 1993

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

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The bacterio-opsin gene was introduced into a "blind" Halobacterium salinarium mutant that (i) lacked all the four retinal proteins [bacteriorhodopsin (BR), halorhodopsin, and sensory rhodopsins (SRs) I and II] and the transducer protein for SRI and (it) showed neither attractant response to long wavelength light nor repellent response to short wavelength light. The resulting transformed cells acquired the capability to sense light stimuli. The cells accumulated in a light spot, demonstrating the BR-mediated orientation in spatial light gradients. As in wild-type cells, a decrease in the intensity oflong wavelength light caused a repellent response by inducing reversals of swimning direction, but, in contrast to wild-type cells, a decrease in the intensity of short wavelength light also repelled the cells. An increase in light intensity evoked an attractant response (i.e., a transient suppression of spontaneous reversals).Signal processing times and adaptation kinetics were similar to the SRI-mediated reactions. However, compared to SRmediated photoresponses, higher light intensities were necessary to induce the BR-mediated responses. The light sensitivity of the transformant was increased by adding 1 mM cyanide and decreased by the addition of arginine, agents that respectively reduce and increase the light-independent generation of the electrochemical potential difference of H+ ions (Ai4*+). A decrease in irradiance to an intensity that was still high enough to saturate BR-initiated AIH+ changes failed to induce the repellent effect, but the addition ofa protonophorous uncoupler sensitized the cell to these light stimuli. The BR D96N mutant (Asp-96 is replaced by Asn) with decreased proton pump activity showed strongly reduced BR-mediated responses. Azide, which increases this mutant's H+ pump efficiency, increased the photosensitivity ofthe mutant cells. Moreover, azide diminished (i) the membrane potential decreasing and (fi) repellent effects of blue light added to the orange background illumination in this mutant. We conclude that the BR-mediated photoreception is due to the light-dependent generation of AFLH+. Our data are consistent with the assumption that the H. salnarium cell monitors the membrane energization level with a "protometer" system measuring total AIH+ changes or its electric potential difference component.Halobacterium salinarium [formerly Halobacterium halobium (1)] contains four retinal proteins: bacteriorhodopsin (BR) (2, 3), halorhodopsin (HR) (4, 5), and sensory rhodopsins (SRs) I and II (6, 7). BR operates as a light-driven H+ pump (2), HR operates as a chloride pump (5), and SRI (6) and SRII (7,8) the cytoplasm via Asp-96. SRs are present in the same cells in much smaller amounts than BR. SRI mediates the attractant effect of the orange and red light, whereas the repellent action of shorter wavelength light is mediated by SRII and the 373-nm intermediate of the SRI photocycle (10). With the discovery of the SRs, operating as highly sensitive photon counters (11), the idea t...

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“…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).…”

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confidence: 99%

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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Negative Phototaxis from Blue Light and the Role of Third Rhodopsinlike Pigment in Halobacterium Cutirubrum

Cited by 23 publications

References 17 publications

A rapid population method for action spectra applied to Halobacterium halobium

A rapid population method for action spectra applied to Halobacterium halobium

Bacteriorhodopsin is involved in halobacterial photoreception.

delta psi-mediated signalling in the bacteriorhodopsin-dependent photoresponse

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