Bioinspired micro/nanomotor with visible light energy–dependent forward, reverse, reciprocating, and spinning schooling motion

In nature, microorganisms could sense the intensity of the incident visible light and exhibit bidirectional (positive or negative) phototaxis. However, it is still challenging to achieve the similar biomimetic phototaxis for the artificial micro/nanomotor (MNM) counterparts with the size from a few nanometers to a few micrometers. In this work, we report a fuel-free carbon nitride (C3N4)/polypyrrole nanoparticle (PPyNP)-based smart MNM operating in water, whose behavior resembles that of the phototactic microorganism. The MNM moves toward the visible light source under low illumination and away from it under high irradiation, which relies on the competitive interplay between the light-induced self-diffusiophoresis and self-thermophoresis mechanisms concurrently integrated into the MNM. Interestingly, the competition between these two mechanisms leads to a collective bidirectional phototaxis of an ensemble of MNMs under uniform illuminations and a spinning schooling behavior under a nonuniform light, both of which can be finely controllable by visible light energy. Our results provide important insights into the design of the artificial counterpart of the phototactic microorganism with sophisticated motion behaviors for diverse applications.

Fold Change Detection in Visual Processing

Visual processing transforms the complexities of the visual world into useful information. Ciona, an invertebrate chordate and close relative of the vertebrates, has one of the simplest nervous systems known, yet has a range of visuomotor behaviors. This simplicity has facilitated studies linking behavior and neural circuitry. Ciona larvae have two distinct visuomotor behaviors – a looming shadow response and negative phototaxis. These are mediated by separate neural circuits that initiate from different clusters of photoreceptors, with both projecting to a CNS structure called the posterior brain vesicle (pBV). We report here that inputs from both circuits are processed to generate fold change detection (FCD) outputs. In FCD, the behavioral response scales with the relative fold change in input, but is invariant to the overall magnitude of the stimulus. Moreover, the two visuomotor behaviors have fundamentally different stimulus/response relationships – indicative of differing circuit strategies, with the looming shadow response showing a power relationship to fold change, while the navigation behavior responds linearly. Pharmacological modulation of the FCD response points to the FCD circuits lying outside of the visual organ (the ocellus), with the pBV being the most likely location. Consistent with these observations, the connectivity and properties of pBV interneurons conform to known FCD circuit motifs, but with different circuit architectures for the two circuits. The negative phototaxis circuit forms a putative incoherent feedforward loop that involves interconnecting cholinergic and GABAergic interneurons. The looming shadow circuit uses the same cholinergic and GABAergic interneurons, but with different synaptic inputs to create a putative non-linear integral feedback loop. These differing circuit architectures are consistent with the behavioral outputs of the two circuits. Finally, while some reports have highlighted parallels between the pBV and the vertebrate midbrain, suggesting a common origin for the two, others reports have disputed this, suggesting that invertebrate chordates lack a midbrain homolog. The convergence of visual inputs at the pBV, and its putative role in visual processing reported here and in previous publications, lends further support to the proposed common origin of the pBV and the vertebrate midbrain.

Characterization of Chlamydomonas reinhardtii Mutants That Exhibit Strong Positive Phototaxis

The most motile phototrophic organisms exhibit photo-induced behavioral responses (photobehavior) to inhabit better light conditions for photosynthesis. The unicellular green alga Chlamydomonas reinhardtii is an excellent model organism to study photobehavior. Several years ago, we found that C. reinhardtii cells reverse their phototactic signs (i.e., positive and negative phototaxis) depending on the amount of reactive oxygen species (ROS) accumulated in the cell. However, its molecular mechanism is unclear. In this study, we isolated seven mutants showing positive phototaxis, even after the induction of negative phototaxis (ap1~7: always positive) to understand the ROS-dependent regulatory mechanism for the phototactic sign. We found no common feature in the mutants regarding their growth, high-light tolerance, and photosynthetic phenotypes. Interestingly, five of them grew faster than the wild type. These data suggest that the ROS-dependent regulation of the phototactic sign is not a single pathway and is affected by various cellular factors. Additionally, the isolation and analyses of mutants with defects in phototactic-sign regulation may provide clues for their application to the efficient cultivation of algae.

A dynein-associated photoreceptor protein prevents ciliary acclimation to blue light

Light-responsive regulation of ciliary motility is known to be conducted through modulation of dyneins, but the mechanism is not fully understood. Here, we report a novel subunit of the two-headed f/I1 inner arm dynein, named DYBLUP, in animal spermatozoa and a unicellular green alga. This subunit contains a BLUF (sensors of blue light using FAD) domain that appears to directly modulate dynein activity in response to light. DYBLUP (dynein-associated BLUF protein) mediates the connection between the f/I1 motor domain and the tether complex that links the motor to the doublet microtubule.Chlamydomonaslacking the DYBLUP ortholog shows both positive and negative phototaxis but becomes acclimated and attracted to high-intensity blue light. These results suggest a mechanism to avoid toxic strong light via direct photoregulation of dyneins.

Basis for the phototaxis sign reversal in the green alga Chlamydomonas reinhardtii studied by high-speed observation

ABSTRACTFor organisms that respond to environmental stimuli using taxes, reversal of the tactic sign should be tightly regulated for survival. The biciliate green alga Chlamydomonas reinhardtii is an excellent model for studying reversal between positive and negative phototaxis. C. reinhardtii cells change swimming direction by modulating the balance of beating forces between their two cilia after photoreception at the eyespot; however, it remains unknown how they reverse phototactic sign. In this study, we observed cells undergoing phototactic turns with a high-speed camera and found that two key factors determine the phototactic sign: which of the two cilia beats stronger for phototactic turning and when the strong beating starts. We developed a mathematical model to explain this sign-reversal with a single equation, which suggests that the timing of the strong ciliary beating is regulated by switching between the light-on and light-off responses at the eyespot.

Response of Mnemiopsis leidyi larvae to light intensity changes

A possible response to light of larvae of Black Sea ctenophore Mnemiopsis leidyi of two age groups (first to fourth day and one-two weeks after hatching) was experimentally studied. The larvae were placed in a Petri dish with seawater, in which two areas (light and dark) were created using a light source and a black opaque background. The number of larvae in each area was recorded for an hour after the start of the experiment. It was found that on average 77 % of the early stage larvae (first to fourth day) migrated to the dark area after an hour. We hypothesized that Mnemiopsis leidyi early stage larvae have negative phototaxis. Similar response of the older larvae (one-two weeks) was not recorded.

Deep origins of chordate midbrain visual processing centers

Ciona larvae have two visuomotor behaviors, a looming shadow response and negative phototaxis. These are mediated by distinct, but overlapping, two-interneuron relay circuits connecting photoreceptors and motor neurons. We report that both behaviors operate via fold-change detection (FCD) mechanisms. In other words, they respond to relative changes in input, meaning that two stimuli of the same fold-change but different by three orders of illumination magnitude give identical behavioral outputs. However, the two behaviors have different response profiles to varying fold-changes, with the negative phototaxis showing a power-function, while the shadow response is linear. The photoreceptors project to putative FCD circuits in the posterior brain vesicle (pBV), but with different circuit architectures for the two behaviors, likely accounting for the differing behavioral responses. Finally, we speculate from similarities in anatomy, gene expression, and connectivity that the pBV has common origins with processing centers of the vertebrate midbrain, including the optic tectum.

The (PATAN)-CheY-Like Response Regulator PixE Interacts with the Motor ATPase PilB1 to Control Negative Phototaxis in the Cyanobacterium Synechocystis sp. PCC 6803

The cyanobacterium Synechocystis sp. PCC 6803 can move directionally on a moist surface toward or away from a light source to reach optimal light conditions for its photosynthetic lifestyle. This behavior, called phototaxis, is mediated by type IV pili (T4P), which can pull a single cell into a certain direction. Several photoreceptors and their downstream signal transduction elements are involved in the control of phototaxis. However, the critical steps of local pilus assembly in positive and negative phototaxis remain elusive. One of the photoreceptors controlling negative phototaxis in Synechocystis is the blue-light sensor PixD. PixD forms a complex with the CheY-like response regulator PixE that dissociates upon illumination with blue light. In this study, we investigate the phototactic behavior of pixE deletion and overexpression mutants in response to unidirectional red light with or without additional blue-light irradiation. Furthermore, we show that PixD and PixE partly localize in spots close to the cytoplasmic membrane. Interaction studies of PixE with the motor ATPase PilB1, demonstrated by in vivo colocalization, yeast two-hybrid and coimmunoprecipitation analysis, suggest that the PixD–PixE signal transduction system targets the T4P directly, thereby controlling blue-light-dependent negative phototaxis. An intriguing feature of PixE is its distinctive structure with a PATAN (PatA N-terminus) domain. This domain is found in several other regulators, which are known to control directional phototaxis. As our PilB1 coimmunoprecipitation analysis revealed an enrichment of PATAN domain response regulators in the eluate, we suggest that multiple environmental signals can be integrated via these regulators to control pilus function.