Yaguchi S et al. (2022), Planktonic sea urchin larvae change their swimm...

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PLoS Genet 2022 Feb 10;182:e1010033. doi: 10.1371/journal.pgen.1010033.

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Planktonic sea urchin larvae change their swimming direction in response to strong photoirradiation.

Yaguchi S , Taniguchi Y , Suzuki H , Kamata M , Yaguchi J .

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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.

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	Fig 1. Sea urchin larvae stop swimming forward and swim backward in response to a light stimulus.(A) Schematic images showing a change in swimming behavior after photoirradiation. The images captured from S3 Video show the changes in the movement of diatom particles around larvae after photoirradiation (cf. Aa to Ab). Ac and Ad show the superimposed images for two seconds each before (Ac) and after (Ad) photoirradiation. The sky-blue rectangle indicates the region of interest (roi) we used for the calculation of particle velocity. Ae and Af show the temporal-color-code mode for the superimposed images. As shown in the indicator, dark blue and bright yellow mark the beginning and end of the 2 sec movie before (Ae) and after (Af) photoirradiation, respectively. (B) Particle velocity measured before and after photoirradiation. N = 6 in each experiment. The velocities of 10 particles were scored for each N. ****, p≤0.0001. (C) Larval arms are required for photoreception. The graph shows the percentages of the larval responses to photoirradiation. The images on each bar graph indicate the micromanipulated larvae used for each experiment. ANE, anterior neuroectoderm.
	Fig 2. Opsin2 expression during embryogenesis.(A) Fluorescent in situ hybridization of Opsin2 mRNA. Although 48-hour-old larvae showed no mRNA signal, 72-hour-old larvae clearly had Opsin2 expression at the tips of their arms. VV, ventral view; DV, dorsal view. (B) Chromogenic in situ hybridization of Opsin2 mRNA in pluteus larvae of H. pulcherrimus and T. reevesii. Bar = 20 μm. The arrows and arrowheads show Opsin2-expressing cells in the postoral arms and preoral arms, respectively. The Opsin2-expressing cells in the preoral arms of T. reevesii are out of focus in this image. (C, D) The expression of Opsin2 was abrogated in larvae in which the secondary mesenchymal cell specifier Gcm (C) or Delta-Notch signal (D) was attenuated. (E) Opsin2 protein was expressed in the same cells expressing Opsin2 mRNA. Green shows serotonergic neurons. Blue in the left image shows the nuclei. The fluorescent image is merged with the brightfield image on the right. (F) Opsin2-expressing cells were close to the ciliary band and neurons. Major neuronal axons, which express the panneural marker synaptotagmin B (SynB), were located beneath the ciliary band.
	Fig 3. Opsin2, which is expressed in mesenchymal cells located in the arms, is required for photoreception.(A) Immunohistochemical analysis of the ChAT protein. The ciliary band neurons in the postoral arms are cholinergic. (inset) In situ hybridization of choline acetyltransferase (ChAT) mRNA in pluteus larvae. (D) The Opsin2 protein was not translated in Opsin2-MO2 morphants. (B) Details of the relationship between Opsin2-expressing cells and cholinergic neurons. The cell processes from Opsin2-expressing cells appear to attach or be closely adjacent to neurons (arrowhead). (C) The Opsin2 protein was expressed in mesenchymal cells in the postoral arms (sky-blue arrow) and preoral arms (sky-blue arrowheads), and it disappeared after morpholino injection (white arrows and arrowheads). (D) The graph shows the difference in particle velocity before vs. after photoirradiation in the presence or absence of the Opsin2 protein. The particle velocity was measured before and after photoirradiation. N = 7 in each experiment. The velocities of 10 particles were measured for each N. , p≤0.05, , p≤0.01, , p≤0.001, **, p≤0.0001, N.S., not significant. (E) Schematic images summarizing the results of this study. Under dark or weak-light conditions (left), the cholinergic system drives forward swimming, but strong photoirradiation (right) stops the cholinergic system via Opsin2.

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