Putative photosensitivity in internal light organs (organs of Pesta) of deep-sea sergestid shrimps.

Many marine species can regulate the intensity of bioluminescence from their ventral photophores in order to counterilluminate, a camouflage technique whereby animals closely match the intensity of the downwelling illumination blocked by their bodies, thereby hiding their silhouettes. Recent studies on autogenic cuticular photophores in deep-sea shrimps indicate that the photophores themselves are light sensitive. Here, our results suggest photosensitivity in a second type of autogenic photophore, the internal organs of Pesta, found in deep-sea sergestid shrimps. Experiments were conducted onboard ship on live specimens, exposing the animals to bright light, which resulted in ultrastructural changes that matched those seen in crustacean eyes during the photoreceptor membrane turnover, a process that is crucial for the proper functioning of photosensitive components. In addition, RNA-seq studies demonstrated the expression of visual opsins and phototransduction genes in photophore tissue that are known to play a role in light detection, and electrophysiological measurements indicated that the light organs are responding to light received by the eyes. The long sought after mechanism of counterillumination remains unknown, but evidence of photosensitivity in photophores may indicate a dual functionality of light detection and emission.

Light organ photosensitivity in deep-sea shrimp may suggest a novel role in counterillumination.

Extraocular photoreception, the ability to detect and respond to light outside of the eye, has not been previously described in deep-sea invertebrates. Here, we investigate photosensitivity in the bioluminescent light organs (photophores) of deep-sea shrimp, an autogenic system in which the organism possesses the substrates and enzymes to produce light. Through the integration of transcriptomics, in situ hybridization and immunohistochemistry we find evidence for the expression of opsins and phototransduction genes known to play a role in light detection in most animals. Subsequent shipboard light exposure experiments showed ultrastructural changes in the photophore similar to those seen in crustacean eyes, providing further evidence that photophores are light sensitive. In many deep-sea species, it has long been documented that photophores emit light to aid in counterillumination - a dynamic form of camouflage that requires adjusting the organ's light intensity to "hide" their silhouettes from predators below. However, it remains a mystery how animals fine-tune their photophore luminescence to match the intensity of downwelling light. Photophore photosensitivity allows us to reconsider the organ's role in counterillumination - not only in light emission but also light detection and regulation.

Author Correction: Light organ photosensitivity in deep-sea shrimp may suggest a novel role in counterillumination.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.