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

Abstract

tom iwanicki 2 , Jamie Sickles 3 & tamara M. frank 3 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. Photoreceptor cells inside the complex eyes of animals are responsible for light detection and subsequent signaling cascades linked to vision. Though light detection in animals is typically associated with ocular photoreceptors, the ability to detect and respond to light can also occur in extraocular tissues and structures 1. Extraocular photoreception has been documented across a range of structures and taxa, including the dermal chromatophores of cephalopods and fish, tube feet of echinoderms, pineal organs in fish and the central nervous systems of arthropods 2-6. Despite the occurrence across diverse metazoans, knowledge regarding the functionality of extraocular photoreceptors remains limited. Bioluminescent light organs, called photophores, provide a unique opportunity to study extraocular photosensitivity, as evidence suggests these structures not only emit light but can also detect it 7. Photophores are complex organs composed of bioluminescent cells (photocytes), and sometimes pigments, reflectors, and filtering structures 8. They can be divided into two types: bacterial or autogenic, where the light is produced by either symbiotic bacteria living within the structure or by the animal itself. In some species, photophores assist in a form of camouflage known as counterillumination. During this process, photophore emissions mimic the downwelling light blocked by the animal's body, thereby camouflaging the animal's profile that would otherwise be detectable to predators below 9,10. Deep-sea shrimp of the family Oplophoridae possess autogenic photophores in three (Systellaspis, Oplophorus and Janicella) of the ten genera 11. Within these three genera, species vertically...

Illuminating the impact of diel vertical migration on visual gene expression in deep‐sea shrimp

“…Also included are the recently recovered r‐opsins from the eye (white triangles) and photophore (black triangles) transcriptomes of the oplophorid J . spinicauda (Bracken‐Grissom et al, 2020) for reference. The putative spectral sensitivities of the r‐opsins clades (short‐wavelength‐, mid‐wavelength (MWS)‐ and long‐wavelength‐sensitive (LWS)) were inferred from these data sets.…”

“…These opsins were near identical to the MWS and LWS opsins recovered in the oplophorid J . spinicauda (Bracken‐Grissom et al, 2020). But, unlike past physiological and behavioural studies on S .…”

“…Tissue‐specific (eye and photophore) reference transcriptomes were assembled de novo with Trinity v2.8.4 (Grabherr et al., 2011; Haas et al., 2013) using in silico read normalization, a minimum contig length of 200 bp and a k‐mer size of 23, which has proven to be the optimal k‐mer size for these crustacean RNA‐seq data sets (i.e. Bracken‐Grissom et al, 2020; Pérez‐Moreno, DeLeo, Palero, & Bracken‐Grissom, 2018). A comprehensive reference assembly containing both tissue types was also assembled for downstream gene expression comparisons between tissue types.…”

“…This suggests opsins are also co‐expressed among the rhabdomeral photoreceptors of some crustaceans. Multiple lines of evidence from a recent study by Bracken‐Grissom et al (2020) also revealed that opsins corresponding to a range of putative spectral sensitivities, and other phototransduction genes, are expressed in the photophores of the oplophorid J . spinicauda ; these bioluminescent light organs are thought to function as extraocular photoreceptors.…”

“…While all species within Oplophoridae have the ability to emit a bioluminescent oral secretion (see Figure 1a) that is used as a defense mechanism to avoid predation (Herring, 1976), only a few genera ( Systellaspis , Janicella and Oplophorus ) possess a secondary light‐producing mechanism in the form of cuticular photophores (Chan et al., 2010; Nowel, Shelton, & Herring, 1998). Photophores are bioluminescent light organs primarily thought to function in counterillumination (Herring, 1976), a form of dynamic camouflage, though recent investigations suggest they are also photosensitive (Bracken‐Grissom et al, 2020). Interestingly, all photophore‐bearing oplophorids participate in diel vertical migrations, where camouflage via counterillumination is particularly useful as they migrate into shallower waters at night to feed.…”