Cyanobacteria use micro-optics to sense light direction

Schuergers, Nils; Lenn, Tchern; Kampmann, Ronald; Meissner, Markus; Esteves, Tiago; Temerinac-Ott, Maja; Korvink, Jan G.; Lowe, Alan R.; Mullineaux, Conrad W.; Wilde, Annegret

doi:10.7554/elife.12620

Cited by 151 publications

(135 citation statements)

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“…These observations appear to have conflicting results because blue light would be expected to work as a "repellent." However, this could be explained by the microoptics effect of the cell, as previously reported (18). When a single cell is exposed to collimated light, the cell condenses the light into the opposite side of the light source because the cell body works as an optics with a diffraction index higher than water.…”

Section: Discussionmentioning

confidence: 62%

“…The blue-light receptor, PixD, mediates the suppression of the T4P dynamics in the opposite region to maintain the above activation. These findings highlight the light-signal processing system in cyanobacteria, which regulates T4P dynamics to navigate cells in a certain direction (18)(19)(20). This concept is in stark contrast to the mechanism of chemotaxis in bacteria, which changes the interval between random swimming and tumbling triggered by repellants (21).…”

mentioning

confidence: 54%

“…Phototaxis of bacteria has been visualized as colony migration on an agar plate (14,22) or as the trajectory of cells (15,18). To observe a detailed trajectory of negative phototaxis at the single-cell level, we constructed an optical setup that allowed us to simultaneously illuminate specimens on a glass substrate both laterally and vertically (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Our experimental setup enables us to evaluate the regulation of T4P filament under an optical microscope on a timescale of minutes and thus could be an ideal tool to quantify the detail of phototactic responses in Synechocystis (14,15,18,31). We also visualized the retraction of T4P by tracking a fluorescent bead that attached to the edge of a single pilus.…”

Section: Discussionmentioning

confidence: 99%

“…When a single cell is exposed to collimated light, the cell condenses the light into the opposite side of the light source because the cell body works as an optics with a diffraction index higher than water. This model was proposed to explain positive phototaxis (18), and we extended the model to negative phototaxis based on the result of direct visualization of T4P and its dynamics. The fact that cell bodies function as an optics was directly confirmed in Chlamydomonas reinhardtii (28).…”

Section: Discussionmentioning

confidence: 99%

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Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria

Nakane

Nishizaka

2017

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

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The type IV pili (T4P) system is a supermolecular machine observed in prokaryotes. Cells repeat the cycle of T4P extension, surface attachment, and retraction to drive twitching motility. Although the properties of T4P as a motor have been scrutinized with biophysics techniques, the mechanism of regulation remains unclear. Here we provided the framework of the T4P dynamics at the single-cell level in Synechocystis sp. PCC6803, which can recognize light direction. We demonstrated that the dynamics was detected by fluorescent beads under an optical microscope and controlled by blue light that induces negative phototaxis; extension and retraction of T4P was activated at the forward side of lateral illumination to move away from the light source. Additionally, we directly visualized each pilus by fluorescent labeling, allowing us to quantify their asymmetric distribution. Finally, quantitative analyses of cell tracking indicated that T4P was generated uniformly within 0.2 min after blue-light exposure, and within the next 1 min the activation became asymmetric along the light axis to achieve directional cell motility; this process was mediated by the photo-sensing protein, PixD. This sequential process provides clues toward a general regulation mechanism of T4P system, which might be essentially common between archaella and other secretion apparatuses.Synechocystis sp. PCC6803 | twitching motility | phototaxis | signal transduction | fluorescence T ype IV pili (T4P) are fascinating supermolecular machines that drive twitching motility, protein secretion, and DNA uptake in prokaryotes (1). Twitching motility is now widely accepted as a form of bacterial translocation involving repetition of the cycle of extension and retraction of the pili (2, 3) (Fig. 1A), which is powered by assembly and disassembly ATPase at the base of helical pilus fibers (4). The mechanical response of a single pilus has been scrutinized in great detail using biophysical approaches such as optical tweezers methodology in Neisseria gonorrheae (3, 5-7), although the dynamic properties resulting from the response to various environmental signals remain less understood than those of bacterial flagella. T4P is also evolutionarily and structurally related to flagella in archaea, which have recently been designated archaella (8-11). Although newly developed techniques enable us to examine the dynamic properties of the machinery, little is known about the regulation mechanism of T4P because tens of components cooperate to orchestrate the dynamics of both the archaella and T4P system. Such complexity hampers the design of an experimental setup with quantitative and reproducible evaluations.To address how the T4P system is activated or repressed by environmental signals over a short timescale, we here used Synechocystis sp. PCC6803, a model cyanobacteria (12)(13)(14). This species exhibits T4P-dependent twitching motility on surfaces such as soft-agar plates at speeds of a few micrometers per minute, and the cell motility direction is regulated both posi...

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Section: Discussionmentioning

confidence: 62%

mentioning

confidence: 54%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria

Nakane

Nishizaka

2017

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

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Photosystems and photoreceptors in cyanobacterial phototaxis and photophobotaxis

Lamparter

2024

FEBS Letters

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Cyanobacteria move by gliding motility on surfaces toward the light or away from it. It is as yet unclear how the light direction is sensed on the molecular level. Diverse photoreceptor knockout mutants have a stronger response toward the light than the wild type. Either the light direction is sensed by multiple photoreceptors or by photosystems. In a study on photophobotaxis of the filamentous cyanobacterium Phormidium lacuna, broad spectral sensitivity, inhibition by 3‐(3,4‐dichlorophenyl)‐1,1‐dimethylurea (DCMU), and a highly sensitive response speaks for photosystems as light direction sensors. Here, it is discussed whether the photosystem theory could hold for phototaxis of other cyanobacteria.

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Phototaxis: Microbial

Storey¹,

Allan²,

Fisher³

2020

Encyclopedia of Life Sciences

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Phototaxis is light‐regulated movement of motile organisms (microorganisms in the case of microbial phototaxis), usually resulting in their attraction to (positive phototaxis) or avoidance of (negative phototaxis) illuminated regions. Bacteria and archaea often use a time‐biased random walk strategy – choosing directions randomly, but moving for longer time periods in the chosen direction if it happens to be correct. They use various photoreceptors, including xanthopsins, bacteriophytochromes and sensory rhodopsins to sense light, and two‐component histidine kinase‐mediated phosphotransfer systems to regulate movement. Eukaryotic microbes, by contrast, can respond to the direction of light by regulating the direction of movement. Their phototransduction pathways involve protein serine/threonine protein kinases and regulation by second messengers. Representative organisms from each of the three taxonomic domains whose photosensory signal transduction pathways have been studied. Many components of the signal transduction pathways controlling phototaxis have been identified, but much remains to be elucidated. Key Concepts Phototaxis enables microorganisms to position themselves in an environment that is optimal for survival. Organisms from all three taxonomic domains display phototaxis with differing photosensory signal transduction pathways. Photosensory signal transduction pathways in eubacteria and archaea involve the coupling of signals from photoreceptors to the same signalling pathways as are used by these organisms for chemotaxis. Phototransduction pathways in archaea and bacteria involve two‐component signalling systems that phosphorylate/dephosphorylate proteins at histidine and aspartate residues. Phototransduction pathways in eukaryotic microbes appear to involve protein phosphorylation/dephosphorylation at serine or threonine residues, and the responsible kinases and phosphatases are regulated by second messengers.

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Cyanobacteria use micro-optics to sense light direction

Cited by 151 publications

References 56 publications

Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria

Asymmetric distribution of type IV pili triggered by directional light in unicellular cyanobacteria

Photosystems and photoreceptors in cyanobacterial phototaxis and photophobotaxis

Phototaxis: Microbial

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