A Novel Molecular Solution for Ultraviolet Light Detection in Caenorhabditis elegans

Abstract

For many organisms the ability to transduce light into cellular signals is crucial for survival. Light stimulates DNA repair and metabolism changes in bacteria, avoidance responses in single-cell organisms, attraction responses in plants, and both visual and nonvisual perception in animals. Despite these widely differing responses, in all of nature there are only six known families of proteins that can transduce light. Although the roundworm Caenorhabditis elegans has none of the known light transduction systems, we show here that C. elegans strongly accelerates its locomotion in response to blue or shorter wavelengths of light, with maximal responsiveness to ultraviolet light. Our data suggest that C. elegans uses this light response to escape the lethal doses of sunlight that permeate its habitat. Short-wavelength light drives locomotion by bypassing two critical signals, cyclic adenosine monophosphate (cAMP) and diacylglycerol (DAG), that neurons use to shape and control behaviors. C. elegans mutants lacking these signals are paralyzed and unresponsive to harsh physical stimuli in ambient light, but short-wavelength light rapidly rescues their paralysis and restores normal levels of coordinated locomotion. This light response is mediated by LITE-1, a novel ultraviolet light receptor that acts in neurons and is a member of the invertebrate Gustatory receptor (Gr) family. Heterologous expression of the receptor in muscle cells is sufficient to confer light responsiveness on cells that are normally unresponsive to light. Our results reveal a novel molecular solution for ultraviolet light detection and an unusual sensory modality in C. elegans that is unlike any previously described light response in any organism.

Principles of designing interpretable optogenetic behavior experiments

“…For example, in Drosophila and C. elegans, light has been shown to drive cellular signaling via newly discovered signaling pathways (Edwards et al 2008;Liu et al 2010;Xiang et al 2010). In C. elegans, reactive oxygen species driven by illumination have been implicated in this signaling (Bhatla and Horvitz 2015).…”

The C. elegans Taste Receptor Homolog LITE-1 Is a Photoreceptor

“…Despite the lack of eyes, C. elegans also responds to light (Edwards et al, 2008;Ward et al, 2008). Specifically, short wavelengths of light, particularly UV light, induce avoidance behavior (negative phototaxis) in C. elegans, which is mediated by a group of photosensory neurons, providing a protective mechanism for the worm to avoid lethal doses of UV in the sunlight (Liu et al, 2010;Ward et al, 2008).…”

An integrated platform enabling optogenetic illumination of Caenorhabditis elegans neurons and muscular force measurement in microstructured environments

“…We hypothesize that this increase in force level is caused by the observed enhanced energetic activity of the worm under intensified illumination. 49,50 In other words, when a worm attempts to avoid strong radiation such as 2500 lumen white light, it tries to excite its body muscles to escape the spot, therefore exerting greater force levels. Meanwhile, the maximum force always occurred when the middle part of the worm body contacted with the sensing pillar, such as reported for the case when no light was projected, 33,51 suggesting that the worm inherently has the strongest muscles in that part and uses them regardless of the environmental situation.…”

“…Due to the smaller size, the force level was too low to be sensed by the pillars, but the worm tracking and light illumination worked well. Because the uncultivated worm exhibits a high sensitivity of avoidance to shortwave beaming, especially blue or ultraviolet light according to previous analysis, 49,50 we first projected blue light to the head/tail segments and observed its locomotion patterns in the LC design. Then, we projected white light and observed its locomotion patterns in HC design, with the main aim to demonstrate the system's capability of providing different environments and illumination patterns.…”