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

Heather D Bracken-Grissom,Megan L Porter,Jamie Sickles,Danielle M Deleo,Tamara M Frank,Tom Iwanicki

doi:10.1038/s41598-020-61284-9

Abstract

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.

Highlights

Extraocular photoreception, the ability to detect and respond to light outside of the eye, has not been previously described in deep-sea invertebrates
Our first approach used RNA sequencing (RNAseq) and phylogenetic methods to search for opsins and phototransduction genes in the photophores, both of which are known to play a role in light detection in most animals[18,19]
Light detection has been demonstrated in the complex bacterial light organs of the squid, Euprymna scolopes, suggesting this may aid the squid in managing symbiont load and/or in comparing ambient light and symbiont light emission www.nature.com/scientificreports

Summary

Introduction

Extraocular photoreception, the ability to detect and respond to light outside of the eye, has not been previously described in deep-sea invertebrates. 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 It remains a mystery how animals fine-tune their photophore luminescence to match the intensity of downwelling light. As animals vertically migrate through the water column or as light intensity changes with photic period, the control of photophore emissions for effective camouflage is crucial This fine-tuning of counterillumination has been experimentally shown in deep-sea shrimp, where the shrimp can alter the intensity, angle and spectral distribution of the light emitted by the photophore[15]. Photophore photosensitivity allows us to reconsider the organ’s role in counterillumination - in light emission and light detection and regulation

Methods

Results

Conclusion