Abstract
To survive, organisms need to precisely respond to various environmental factors, such as light and gravity. Among these, light is so important for most life on Earth that light-response systems have become extraordinarily developed during evolution, especially in multicellular animals. A combination of photoreceptors, nervous system components, and effectors allows these animals to respond to light stimuli. In most macroscopic animals, muscles function as effectors responding to light, and in some microscopic aquatic animals, cilia play a role. It is likely that the cilia-based response was the first to develop and that it has been substituted by the muscle-based response along with increases in body size. However, although the function of muscle appears prominent, it is poorly understood whether ciliary responses to light are present and/or functional, especially in deuterostomes, because it is possible that these responses are too subtle to be observed, unlike muscle responses. Here, we show that planktonic sea urchin larvae reverse their swimming direction due to the inhibitory effect of light on the cholinergic neuron signaling>forward swimming pathway. We found that strong photoirradiation of larvae that stay on the surface of seawater immediately drives the larvae away from the surface due to backward swimming. When Opsin2, which is expressed in mesenchymal cells in larval arms, is knocked down, the larvae do not show backward swimming under photoirradiation. Although Opsin2-expressing cells are not neuronal cells, immunohistochemical analysis revealed that they directly attach to cholinergic neurons, which are thought to regulate forward swimming. These data indicate that light, through Opsin2, inhibits the activity of cholinergic signaling, which normally promotes larval forward swimming, and that the light-dependent ciliary response is present in deuterostomes. These findings shed light on how light-responsive tissues/organelles have been conserved and diversified during evolution.
Highlights
The importance of light for organisms on Earth has led to the extraordinary development of sophisticated light-response systems during evolution
Light regulates the swimming behavior of sea urchin larvae ciliary responses were initially acquired in unicellular and small multicellular organisms, but the pathway is poorly understood in deuterostomes, whose behavior mostly depends on responses involving muscle
It is unclear whether ciliary responses to light are present and/or functional in deuterostomes since these responses may be too subtle for observation, unlike muscle responses
Summary
It is essential for organisms to precisely respond to extrinsic signals, such as light, gravity, and temperature. Even single-celled organisms, such as Chlamydomonas, change the beating pattern of cilia/flagella when photoirradiated [1] As another example, another group of nonmetazoans, the choanoflagellates, show response behaviors to light input [2]. Stronger UV light induces deeper migration of Daphnia [3–5] As photoreceptors for these metazoan behaviors, opsin family members function mainly to receive light of a specific wavelength and transmit the signal to downstream systems [6, 7]. In the planktonic larvae of flatworms, Annelida, and Mollusca, responses to light are supported mainly by changes in ciliary beating, with which the larvae show reflex behavior and/or phototaxis [16–18] This cilia-based response to light is found in cnidarian and sponge larvae [19, 20], it is expected that the sponge lineage lost Opsin genes [8]. Nematodes and arthropods have lost motile cilia in their clades and have no cilia-based responses
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