Discovery and characterization of Hv1-type proton channels in reef-building corals.

Gisela Rangel-Yescas,Anastazia T Banaszak,Ernesto Maldonado,Leon D Islas,Tamara Rosenbaum,Esteban Suárez-Delgado,Cecilia Cervantes,Miguel A Cervantes-Rocha,Ian Scott Ramsey

doi:10.7554/elife.69248

Gisela Rangel-Yescas, Anastazia T Banaszak + Show 7 more

Open Access

https://doi.org/10.7554/elife.69248

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Abstract

Voltage-dependent proton-permeable channels are membrane proteins mediating a number of important physiological functions. Here we report the presence of a gene encoding Hv1 voltage-dependent, proton-permeable channels in two species of reef-building corals. We performed a characterization of their biophysical properties and found that these channels are fast-activating and modulated by the pH gradient in a distinct manner. The biophysical properties of these novel channels make them interesting model systems. We have also developed an allosteric gating model that provides mechanistic insight into the modulation of voltage-dependence by protons. This work also represents the first functional characterization of any ion channel in scleractinian corals. We discuss the implications of the presence of these channels in the membranes of coral cells in the calcification and pH-regulation processes and possible consequences of ocean acidification related to the function of these channels.

Highlights

Scleractinian or stony corals are organisms in the phylum Cnidaria that deposit calcium carbonate in the form of aragonite to build an exoskeleton
The extracellular histidine residues involved in Zn2+ coordination are present. These results suggest that our sequence is that of a bona fide Hv1 voltage-sensing domain (VSD)
The presence of Hv1 sequences in many other species of corals from disparate clades, suggest that Hv1 plays an important role in coral physiology

Summary

Introduction

Scleractinian or stony corals are organisms in the phylum Cnidaria that deposit calcium carbonate in the form of aragonite to build an exoskeleton. Coral reefs act as natural barriers from strong ocean currents, waves and tropical storms, providing coastal protection This protection centers on the ability of scleractinian corals to produce enough calcium carbonate (CaCO3). Calcification by scleractinian corals is a process that has been shown to be modulated by the pH of the solution in which calcium carbonate is precipitated (Allemand et al, 2011). To this end, corals produce a specialized compartment between the ectoderm and the external substrate or skeleton called calicoblastic compartment, which contains a fluid derived from the surrounding sea water. We hypothesized that proton channels might be fundamental to this physiological process and required for calcification in hard corals

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