Characterization of TRPA channels in the starfish Patiria pectinifera: involvement of thermally activated TRPA1 in thermotaxis in marine planktonic larvae

Shigeru Saito,Makoto Tominaga,Ryohei Furukawa,Gen Hamanaka,Jun Gojobori,Hiroyuki Kaneko,Narudo Kawai,Yoko Satta

doi:10.1038/s41598-017-02171-8

Abstract

The vast majority of marine invertebrates spend their larval period as pelagic plankton and are exposed to various environmental cues. Here we investigated the thermotaxis behaviors of the bipinnaria larvae of the starfish, Patiria pectinifera, in association with TRPA ion channels that serve as thermal receptors in various animal species. Using a newly developed thermotaxis assay system, we observed that P. pectinifera larvae displayed positive thermotaxis toward high temperatures, including toward temperatures high enough to cause death. In parallel, we identified two TRPA genes, termed PpTRPA1 and PpTRPA basal, from this species. We examined the phylogenetic position, spatial expression, and channel properties of each PpTRPA. Our results revealed the following: (1) The two genes diverged early in animal evolution; (2) PpTRPA1 and PpTRPA basal are expressed in the ciliary band and posterior digestive tract of the larval body, respectively; and (3) PpTRPA1 is activated by heat stimulation as well as by known TRPA1 agonists. Moreover, knockdown and rescue experiments demonstrated that PpTRPA1 is involved in positive thermotaxis in P. pectinifera larvae. This is the first report to reveal that TRPA1 channels regulate the behavioral response of a marine invertebrate to temperature changes during its planktonic larval period.

Highlights

The vast majority of marine invertebrates spend their larval period as pelagic plankton and are exposed to various environmental cues
We found that PpTRPA1 and PpTRPA basal are expressed differently in P. pectinifera larvae: the former is expressed in the ciliary band, and the latter is concentrated in the posterior region of the digestive tract
Our results suggest that PpTRPA1 is involved in positive thermotaxis in P. pectinifera larvae

Summary

Introduction

The vast majority of marine invertebrates spend their larval period as pelagic plankton and are exposed to various environmental cues. We investigated the thermotaxis behaviors of the bipinnaria larvae of the starfish, Patiria pectinifera, in association with TRPA ion channels that serve as thermal receptors in various animal species. Knockdown and rescue experiments demonstrated that PpTRPA1 is involved in positive thermotaxis in P. pectinifera larvae This is the first report to reveal that TRPA1 channels regulate the behavioral response of a marine invertebrate to temperature changes during its planktonic larval period. By using infrared or visible light isolation filters, we further found that starfish larvae are attracted to infrared radiation, suggesting that they possess an ability to perform positive thermotaxis toward warmth These findings provide the opportunity to investigate how planktonic larvae actively respond to environmental cues such as temperatures. Ten thermoTRP channels have been identified and further classified into three subfamilies (TRPV, TRPM, and TRPA)[14,15,16], and several homologous genes to these thermoTRP channels have been identified in a wide variety of animal species including vertebrates, insects, and even cnidarians[19,20,21,22]

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