RESUMEN
The currently unsurpassed diversity of photoreceptors found in the eyes of stomatopods, or mantis shrimps, is achieved through a variety of opsin-based visual pigments and optical filters. However, the presence of extraocular photoreceptors in these crustaceans is undescribed. Opsins have been found in extraocular tissues across animal taxa, but their functions are often unknown. Here, we show that the mantis shrimp Neogonodactylus oerstedii has functional cerebral photoreceptors, which expands the suite of mechanisms by which mantis shrimp sense light. Illumination of extraocular photoreceptors elicits behaviors akin to common arthropod escape responses, which persist in blinded individuals. The anterior central nervous system, which is illuminated when a mantis shrimp's cephalothorax protrudes from its burrow to search for predators, prey, or mates, appears to be photosensitive and to feature two types of opsin-based, potentially histaminergic photoreceptors. A pigmented ventral eye that may be capable of color discrimination extends from the cerebral ganglion, or brain, against the transparent outer carapace, and exhibits a rapid electrical response when illuminated. Additionally, opsins and histamine are expressed in several locations of the eyestalks and cerebral ganglion, where any photoresponses could contribute to shelter-seeking behaviors and other functions.
Asunto(s)
Decápodos/metabolismo , Animales , Encéfalo/metabolismo , Ganglión/metabolismo , Histamina/metabolismo , Opsinas/metabolismo , Células Fotorreceptoras de Vertebrados/metabolismoRESUMEN
Most stomatopod crustaceans have complex retinas in their compound eyes, with up to 16 spectral types of photoreceptors, but members of the superfamily Squilloidea have much simpler retinas, thought to contain a single photoreceptor spectral class. In the Atlantic stomatopod Squilla empusa, microspectrophotometry shows that all photoreceptors absorb light maximally at 517 nm, indicating that a single visual pigment is present in all photoreceptors in the retina. However, six distinct, but partial, long wavelength sensitive (LWS) opsin transcripts, which encode the protein component of the visual pigment, have been previously isolated through RT-PCR. In order to investigate the spectral and functional differences among S. empusa's opsins, we used RT-PCR to complete the 3' end of sequences for five of the six expressed opsins. The extended sequences spanned from the first transmembrane (TM1) helix to the 3' end of the coding region. Using homology-based modeling, we predicted the three-dimensional structure of the amino acid translation of the S. empusa opsins. Based on these analyses, S. empusa LWS opsins share a high sequence identity in TM regions and in amino acids within 15 Å of the chromophore-binding lysine on TM helix 7 (TM7), suggesting that these opsins produce spectrally similar visual pigments in agreement with previous results. However, we propose that these spectrally similar opsins differ functionally, as there are non-conservative amino acid substitutions found in intracellular loop 2 (ICL2) and TM5/ICL3, which are critical regions for G-protein binding, and substitutions in extracellular regions suggest different chromophore attachment affinities. In situ hybridization of two of the opsins (Se5 and Se6) revealed strong co-expression in all photoreceptors in both midband and peripheral regions of the retina as well as in selected ocular and cerebral ganglion neuropils. These data suggest the expression of multiple opsins-likely spectrally identical, but functionally different-in multiple types of neuronal cells in S. empusa. This suggests that the multiple opsins characteristic of other stomatopod species may have similar functional specialization.
Asunto(s)
Proteínas de Artrópodos/genética , Crustáceos/genética , Ojo/metabolismo , Expresión Génica , Opsinas/genética , Secuencia de Aminoácidos , Animales , Proteínas de Artrópodos/química , Proteínas de Artrópodos/metabolismo , Crustáceos/metabolismo , Perfilación de la Expresión Génica , Opsinas/química , Opsinas/metabolismo , Alineación de SecuenciaRESUMEN
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 Gq-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.