Dissecting the Determinants of Light Sensitivity in Amphioxus Microvillar Photoreceptors: Possible Evolutionary Implications for Melanopsin Signaling

Abstract

Melanopsin, a photopigment related to the rhodopsin of microvillar photoreceptors of invertebrates, evolved in vertebrates to subserve nonvisual light-sensing functions, such as the pupillary reflex and entrainment of circadian rhythms. However, vertebrate circadian receptors display no hint of a microvillar specialization and show an extremely low light sensitivity and sluggish kinetics. Recently in amphioxus, the most basal chordate, melanopsin-expressing photoreceptors were characterized; these cells share salient properties with both rhabdomeric photoreceptors of invertebrates and circadian receptors of vertebrates. We used electrophysiology to dissect the gain of the light-transduction process in amphioxus and examine key features that help outline the evolutionary transition toward a sensor optimized to report mean ambient illumination rather than mediating spatial vision. By comparing the size of current fluctuations attributable to single photon melanopsin isomerizations with the size of single-channels activated by light, we concluded that the gain of the transduction cascade is lower than in rhabdomeric receptors. In contrast, the expression level of melanopsin (gauged by measuring charge displacements during photo-induced melanopsin isomerization) is comparable with that of canonical visual receptors. A modest amplification in melanopsin-using receptors is therefore apparent in early chordates; the decrease in photopigment expression-and loss of the anatomical correlates-observed in vertebrates subsequently enabled them to attain the low photosensitivity tailored to the role of circadian receptors.

Retinal Attachment Instability Is Diversified among Mammalian Melanopsins

“…3D). Consistent with the above hypothesis, amphioxus Hesse and Joseph photoreceptor cells, in which the melanopsin functions as a photopigment (16), show a high photosensitivity comparable to visual photoreceptor cells (65), in contrast to ipRGCs in mammals.…”

Amphioxus photoreceptors - insights into the evolution of vertebrate opsins, vision and circadian rhythmicity

“…The physiology and phototransduction cascade in isolated DO and JCs has been investigated in several studies (Acemel et al, 2016;Angueyra et al, 2012;Ferrer et al, 2012;Gomez Mdel et al, 2009;Nasi and del Pilar Gomez, 2009;Peinado et al, 2015;Pulido et al, 2012). These seminal studies not only confirmed that JCs and DO indeed function as photoreceptors, but also provided comparative data with respect to invertebrate rhabdomeric photoreceptors and ipRGCs.…”

Comparison of the isomerization mechanisms of human melanopsin and invertebrate and vertebrate rhodopsins

“…The different studies carried out so far on melanopsin light sensitivity do not lead to consistent results. Although Do et al (14) argue that ipRGCs work at extremely low irradiation intensities showing a single-photon response larger than rods, Ferrer et al (15) conclude that the melanopsin has a reduced sensitivity relative to visual pigments. On the other hand, these photoreceptors would be expected to display high light sensitivity (14).…”