Mechanism Of Phototaxis Research Articles

Phototactic signaling network in rod-shaped cyanobacteria: A study on Synechococcus elongatus UTEX 3055

Light-controlled motility is advantageous for photosynthetic prokaryotes to better survive in environment with constantly changing light conditions. For cyanobacteria, light is both an energy source for photosynthesis and a stress factor. Consequently, some cyanobacteria evolved the ability to control type-IV pili (T4P)-mediated surface motility using a chemotaxis-like system in response to light signals. Extensive studies on the mechanism of phototaxis has been conducted in the spherical Synechocystis sp. PCC 6803 and the filamentous strain Nostoc punctiforme, while less is explored in rod-shaped cyanobacteria such as Synechococcus species. In this study, we investigated the phototaxis pathway in the unicellular rod-shaped cyanobacterium Synechococcus elongatus UTEX 3055, which exhibits bidirectional phototaxis using a single tax1 operon, in contrast to more complex and multiple gene clusters revealed in Synechocystis sp. PCC 6803. Results obtained by protein-protein interaction assays and protein subcellular localization experiments indicated that proteins encoded by the tax1 operon form large clusters that asymmetrically distributed both between the two poles and within the same pole. In vitro phosphorylation assays and site-directed mutations of conserved phosphorylation sites in PixLSe, PixGSe and PixHSe demonstrate that PixLSe acts as a histidine kinase, and PixGSe and PixHSe as response regulators for signal transduction. We further show that PixGSe and PixHSe are recruited to cell poles via interactions with the N-terminal region of PixLSe. While phosphotransfer reactions in this signaling pathway are critical for phototactic signaling, the two response regulators appear to play different roles in the control of phototaxis. This study provides a framework for further investigation into the complex phototactic signaling network in rod-shaped cyanobacteria with clearly defined cell poles in contrast to round shaped Synechocystis species with virtual cells poles through light-lensing effect.

Phototaxis of Chlamydomonas arises from a tuned adaptive photoresponse shared with multicellular Volvocine green algae.

A fundamental issue in biology is the nature of evolutionary transitions from unicellular to multicellular organisms. Volvocine algae are models for this transition, as they span from the unicellular biflagellate Chlamydomonas to multicellular species of Volvox with up to 50,000 Chlamydomonas-like cells on the surface of a spherical extracellular matrix. The mechanism of phototaxis in these species is of particular interest since they lack a nervous system and intercellular connections; steering is a consequence of the response of individual cells to light. Studies of Volvox and Gonium, a 16-cell organism with a plate-like structure, have shown that the flagellar response to changing illumination of the cellular photosensor is adaptive, with a recovery time tuned to the rotation period of the colony around its primary axis. Here, combining high-resolution studies of the flagellar photoresponse of micropipette-held Chlamydomonas with 3D tracking of freely swimming cells, we show that such tuning also underlies its phototaxis. A mathematical model is developed based on the rotations around an axis perpendicular to the flagellar beat plane that occur through the adaptive response to oscillating light levels as the organism spins. Exploiting a separation of timescales between the flagellar photoresponse and phototurning, we develop an equationof motion that accurately describes the observed photoalignment. In showing that the adaptive timescales in Volvocine algae are tuned to the organisms' rotational periods across three orders of magnitude in cell number, our results suggest a unified picture of phototaxis in green algae in which the asymmetry in torques that produce phototurns arise from the individual flagella of Chlamydomonas, the flagellated edges of Gonium, and the flagellated hemispheres of Volvox.

Green Algae as Model Organisms for Biological Fluid Dynamics.

In the past decade the volvocine green algae, spanning from the unicellular Chlamydomonas to multicellular Volvox, have emerged as model organisms for a number of problems in biological fluid dynamics. These include flagellar propulsion, nutrient uptake by swimming organisms, hydrodynamic interactions mediated by walls, collective dynamics and transport within suspensions of microswimmers, the mechanism of phototaxis, and the stochastic dynamics of flagellar synchronization. Green algae are well suited to the study of such problems because of their range of sizes (from 10 μm to several millimetres), their geometric regularity, the ease with which they can be cultured and the availability of many mutants that allow for connections between molecular details and organism-level behavior. This review summarizes these recent developments and highlights promising future directions in the study of biological fluid dynamics, especially in the context of evolutionary biology, that can take advantage of these remarkable organisms.

Expression Dynamics and Protein Localization of Rhabdomeric Opsins in Platynereis Larvae

The larval stages of polychaete annelids are often responsive to light and can possess one to six eyes. The early trochophore larvae of the errant annelid Platynereis dumerilii have a single pair of ventral eyespots, whereas older nectochaete larvae have an additional two pairs of dorsal eyes that will develop into the adult eyes. Early Platynereis trochophores show robust positive phototaxis starting on the first day of development. Even though the mechanism of phototaxis in Platynereis early trochophore larvae is well understood, no photopigment (opsin) expression has yet been described in this stage. In late trochophore larvae, a rhabdomeric-type opsin, r-opsin1, expressed in both the eyespots and the adult eyes has already been reported. Here, we identify another Platynereis rhabdomeric opsin, r-opsin3, that is expressed in a single photoreceptor in the eyespots in early trochophores, suggesting that it mediates early larval phototaxis. We also show that r-opsin1 and r-opsin3 are expressed in adjacent photoreceptor cells in the eyespots in later stages, indicating that a second eyespot-photoreceptor differentiates in late trochophore larvae. Using serial transmission electron microscopy (TEM), we identified and reconstructed both photoreceptors and a pigment cell in the late larval eyespot. We also characterized opsin expression in the adult eyes and found that the two opsins co-express there in several photoreceptor cells. Using antibodies recognizing r-opsin1 and r-opsin3 proteins, we demonstrate that both opsins localize to the rhabdomere in all six eyes. In addition, we found that r-opsin1 mRNA is localized to, and translated in, the projections of the adult eyes. The specific changes we describe in opsin transcription and translation and in the cellular complement suggest that the six larval eyes undergo spectral and functional maturation during the early planktonic phase of the Platynereis life cycle.

Mechanism of phototaxis in marine zooplankton

The simplest animal eyes are eyespots composed of two cells only: a photoreceptor and a shading pigment cell. They resemble Darwin's 'proto-eyes', considered to be the first eyes to appear in animal evolution. Eyespots cannot form images but enable the animal to sense the direction of light. They are characteristic for the zooplankton larvae of marine invertebrates and are thought to mediate larval swimming towards the light. Phototaxis of invertebrate larvae contributes to the vertical migration of marine plankton, which is thought to represent the biggest biomass transport on Earth. Yet, despite its ecological and evolutionary importance, the mechanism by which eyespots regulate phototaxis is poorly understood. Here we show how simple eyespots in marine zooplankton mediate phototactic swimming, using the marine annelid Platynereis dumerilii as a model. We find that the selective illumination of one eyespot changes the beating of adjacent cilia by direct cholinergic innervation resulting in locally reduced water flow. Computer simulations of larval swimming show that these local effects are sufficient to direct the helical swimming trajectories towards the light. The computer model also shows that axial rotation of the larval body is essential for phototaxis and that helical swimming increases the precision of navigation. These results provide, to our knowledge, the first mechanistic understanding of phototaxis in a marine zooplankton larva and show how simple eyespots regulate it. We propose that the underlying direct coupling of light sensing and ciliary locomotor control was a principal feature of the proto-eye and an important landmark in the evolution of animal eyes.

Gain setting in Chlamydomonas reinhardtii: Mechanism of phototaxis and the role of the photophobic response

The unicellular green alga (Chlamydomonas reinhardtii maintains sensitivity of its phototaxis response (alignment of swimming direction along the axis of a light beam) over several orders of magnitude of light intensities. It is widely accepted that the rotation of the swimming cell provides temporal comparisons of light intensities via periodic contrast generated by its asymmetrically positioned refractile eyespot organelle. The cells also exhibit a second behavioral response to light called the photophobic (or stop) response, which is a brief cessation of swimming caused by a temporal change in light intensity. The cells are desensitized to photophobic stimuli by light exposure. Through comparative measurements of both responses, we explain the behavioral basis of the large dynamic range of phototaxis in terms of precise desensitization of the photophobic response. The basis of the explanation is that the flagellar beat changes which cause phototactic orientation are the residual of the photophobic response after desensitization (i.e., "mini-photophobic" reactions which cause brief reorienting motions without a full stop). This interpretation predicts quantitatively the dependence of the extent of desensitization on light intensity and the dependence of onset and maintenance of phototaxis on extent of desensitization. These predictions are tested and confirmed in this report.

A one-instant mechanism of phototaxis in the cyanobacteriumPhormidium uncinatum

The front portion (‘head’) of a Phormidium uncinatum trichome responds to a step-down in light intensity [10], whereas the rear end (‘tail’) responds to step-up stimuli [11]. We studied this phenomenon further and found that: (i) illumination of the head caused a reversal within 1 min in only 6% of the trichomes, whereas illumination of the tail produced a reversal in 56% of trichomes; (ii) if a light spot trained on the head of a trichome was moved together with the trichome, there were no reversals for > 20 min, while the normal rate of spontaneous reversals was once per 3–5 min. Shifting the light spot from the head to the tail caused a reversal within 1–2 min; (iii) both the step-up response of the tail and phototaxis were suppressed by an inhibitor of methylation, ethionine, but not by inhibitors of photosynthesis (DCMU, DBMIB); phototaxis and the step-up response of the tail were absent in red light (λ > 670 nm). It was concluded that trichomes of P. uncinatum possess a one-instant mechanism of phototaxis, which involves a simultaneous comparison of light intensities between two parts of the organism.