Sea urchin larvae utilize light for regulating the pyloric opening

Junko Yaguchi,Shunsuke Yaguchi

doi:10.1186/s12915-021-00999-1

Abstract

BackgroundLight is essential for various biological activities. In particular, visual information through eyes or eyespots is very important for most of animals, and thus, the functions and developmental mechanisms of visual systems have been well studied to date. In addition, light-dependent non-visual systems expressing photoreceptor Opsins have been used to study the effects of light on diverse animal behaviors. However, it remains unclear how light-dependent systems were acquired and diversified during deuterostome evolution due to an almost complete lack of knowledge on the light-response signaling pathway in Ambulacraria, one of the major groups of deuterostomes and a sister group of chordates.ResultsHere, we show that sea urchin larvae utilize light for digestive tract activity. We found that photoirradiation of larvae induces pyloric opening even without addition of food stimuli. Micro-surgical and knockdown experiments revealed that this stimulating light is received and mediated by Go(/RGR)-Opsin (Opsin3.2 in sea urchin genomes) cells around the anterior neuroectoderm. Furthermore, we found that the anterior neuroectodermal serotoninergic neurons near Go-Opsin-expressing cells are essential for mediating light stimuli-induced nitric oxide (NO) release at the pylorus. Our results demonstrate that the light>Go-Opsin>serotonin>NO pathway functions in pyloric opening during larval stages.ConclusionsThe results shown here will lead us to understand how light-dependent systems of pyloric opening functioning via neurotransmitters were acquired and established during animal evolution. Based on the similarity of nervous system patterns and the gut proportions among Ambulacraria, we suggest the light>pyloric opening pathway may be conserved in the clade, although the light signaling pathway has so far not been reported in other members of the group. In light of brain-gut interactions previously found in vertebrates, we speculate that one primitive function of anterior neuroectodermal neurons (brain neurons) may have been to regulate the function of the digestive tract in the common ancestor of deuterostomes. Given that food consumption and nutrient absorption are essential for animals, the acquirement and development of brain-based sophisticated gut regulatory system might have been important for deuterostome evolution.

Highlights

Light is essential for various biological activities
The average pyloric opening time among individuals was approximately 1.5 min (n = 8, Additional file 1: Fig. S1), and the pylori of more than 40% of the larval population opened in response to the light stimulus (Fig. 1b; see the figure legend for the calculation)
The reason why only 40% of the larvae responded to light will be elucidated in the future. This ratio jumped to more than 80% with food (Additional file 1: Fig. S3), indicating that food stimulation represents another regulatory pathway that activates the digestive tract, we did not focus on this pathway in this paper

Summary

Introduction

Light is essential for various biological activities. In particular, visual information through eyes or eyespots is very important for most of animals, and the functions and developmental mechanisms of visual systems have been well studied to date. Recent studies have suggested that non-visual systems dependent on light play essential roles in the life activities of animal, such as circadian rhythms [6, 7]. Many of these light-dependent systems rely on photoreceptor Opsin members, which belong to the group of sensory G-protein-coupled receptors (GPCRs), and their functional diversity has led us to consider how visual/non-visual systems developed during evolution to utilize light as an external signaling source [8,9,10]. It is still difficult to precisely compare the functions of and predict the evolution of the light-dependent system in deuterostomes because we do not have experimental data about the precise function of the Opsin family in Ambulacraria, a sister group of chordates, the evolutionary comparisons based on the primary structures have been performed [13]

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Discussion

Conclusion