Here we establish that, contrary to expectations, Caenorhabditis elegans nematode worms possess a color discrimination system despite lacking any opsin or other known visible light photoreceptor genes. We found that white light guides C. elegans foraging decisions away from harmful bacteria that secrete a blue pigment toxin. Absorption of amber light by this blue pigment toxin alters the color of light sensed by the worm, and thereby triggers an increase in avoidance. By combining narrow-band blue and amber light sources, we demonstrated that detection of the specific blue:amber ratio by the worm guides its foraging decision. These behavioral and psychophysical studies thus establish the existence of a color detection system that is distinct from those of other animals.3
Main text:C. elegans live in decomposing organic matter where they feed on microorganisms 1-3 , some of which secrete colorful pigments. While C. elegans lack any specialized photoreceptor cells or opsin genes, they possess an illuminance sensing system that mediates rapid escape responses to short-wavelength light 4-6 . However, it is unknown whether C. elegans use light information, potentially including color, to inform complex decisions like foraging in environments containing colorful food sources. To address this question, we first tested whether white light alters foraging decisions on P. aeruginosa bacterial lawns containing the blue pigment toxin pyocyanin, one of a number of small molecule phenazine toxins secreted by P. aeruginosa 7-10 . We employed an 8 kilolux LED array white light source to mimic naturalistic lighting levels (Fig. 1a, Supplementary Fig. 1a). Previous studies have shown that foraging decisions to remain on or leave a bacterial lawn are guided by a variety of factors 11,12 . Worms remain on bacterial lawns that are easy to eat and support growth, while leaving lawns that are of poor nutritive quality, repulsive, or pathogenic [11][12][13][14][15][16] . Worms are initially attracted to P. aeruginosa lawns, but over a time course of hours, as the P. aeruginosa continues to divide and secrete toxins, they respond to its increasingly aversive qualities and begin to leave 14,15,[17][18][19][20] .Whether light plays a role in guiding avoidance of P. aeruginosa has never been tested. Here we employed a standard lawn avoidance assay, placing worms on a P. aeruginosa lawn in the center of an agar plate, and quantified the time course of avoidance as the fraction of worms found off the lawn (Fig. 1a). Consistent with prior studies, worms gradually avoid P. aeruginosa strain PA14 over a span of many hours 14,15,[17][18][19][20] (Fig. 1a). Surprisingly, however, this avoidance is dramatically potentiated by white light (Fig. 1b). White light does not potentiate avoidance of