Opsin Expression in the Central Nervous System of the Mantis Shrimp Neogonodactylus oerstedii

Abstract

Visual pigments, each composed of an opsin protein covalently bound to a chromophore molecule, confer light sensitivity for vision. The eyes of some species of stomatopod crustaceans, or mantis shrimp, can express dozens of different opsin genes. The opsin diversity, along with spectral filters and unique tripartite eye structure, bestow upon stomatopods unusually complex visual systems. Although opsins are found in tissues outside typical image-forming eyes in other animals, extraocular opsin expression in stomatopods, animals well known for their diversity of opsins, was unknown. Caudal photoreception in the central nervous system of decapod crustaceans, a group closely related to stomatopod crustaceans, is thought to be opsin based. However, electrophysiological data suggest that stomatopods do not have caudal photoreceptors. In this study, we identified mRNAs that could encode four different opsins and several components of a potential G-mediated phototransduction pathway in the central nervous system of the Caribbean mantis shrimp Neogonodactylus oerstedii. The four opsins are abundantly expressed in the cerebral ganglion, or brain, with little or no expression in the remainder of the ventral nerve cord. Our data suggest that there are previously undiscovered cerebral photoreceptors in stomatopods.

Cerebral photoreception in mantis shrimp

“…Following our observations of light-induced behaviors in eyeless mantis shrimp, and the identification of a photosensitive ventral eye, we investigated the expression patterns of opsins potentially used to produce light sensitive visual pigments in mantis shrimp extraocular photoreceptors. Our previous transcriptomic analyses revealed that four opsin transcripts—one middle-wavelength-sensitive (MWS) and three long-wavelength-sensitive (LWS) opsins—are expressed in the CG of N. oerstedii 21 . Therefore, we labeled mantis shrimp eyestalk and CG tissues using gene-specific in situ probes to visualize the expression of these four identified opsin transcripts.…”

“…The NoLWS1 opsin riboprobe labels the dorsal and ventral hemispheres of the retina, likely labeling transcripts of No14, an opsin transcript sequence that was isolated from the eye of N. oerstedii 18 and has the same 3′ untranslated region (3′-UTR) sequence (see ref. 21 for sequence alignment). In the CG, NoMWS1 and NoLWS3 opsin transcripts are coexpressed in the ventral eye, and NoLWS1 and NoLWS2 opsin transcripts are expressed in cell bodies, including those in the olfactory lobe (Fig.…”

“…Since then, the arthropod central complex has been compared to the vertebrate basal ganglia, affecting behavior in the form of motor output, memory formation, attention, and sleep 30 . As we recently suggested 21 , information from opsin-based extraocular photoreceptors could be integrated with other sensory input in the central complex (or elsewhere) to affect various aspects of an animal’s physiology. Observed opsin expression patterns in mantis shrimp are consistent with this hypothesis.…”

“…Custom genes designed against the 3′-UTR of the four opsins identified by Donohue et al . 21 , flanked by restriction enzyme and polymerase sites, were transformed into DH5α Escherichia coli bacteria. The sequences used as templates to label NoMWS1, NoLWS1, NoLWS2, and NoLWS3 are provided in Supplementary Table S1 .…”

“…The large number of opsins expressed in the eyes, and the resulting diversity of photoreceptors, is thought to reflect rampant gene duplications 18 . We recently found four opsins that are expressed in the CG of adult mantis shrimp ( Neogonodactylus oerstedii ) 21 . However, it was unknown whether or not functional photoreceptors exist in the CG or elsewhere in the central nervous system.…”