Divalent metal transporter-related protein restricts animals to marine habitats

Mieko Sassa,Toshiyuki Takagi,Kotaro Shirai,Koji Inoue,Yuki Yoshioka,Naoko Murakami-Sugihara,Chuya Shinzato,Azusa Kinjo,Yuna Zayasu,Shinji Kanda

doi:10.1038/s42003-021-01984-8

Abstract

Utilization and regulation of metals from seawater by marine organisms are important physiological processes. To better understand metal regulation, we searched the crown-of-thorns starfish genome for the divalent metal transporter (DMT) gene, a membrane protein responsible for uptake of divalent cations. We found two DMT-like sequences. One is an ortholog of vertebrate DMT, but the other is an unknown protein, which we named DMT-related protein (DMTRP). Functional analysis using a yeast expression system demonstrated that DMT transports various metals, like known DMTs, but DMTRP does not. In contrast, DMTRP reduced the intracellular concentration of some metals, especially zinc, suggesting its involvement in negative regulation of metal uptake. Phylogenetic distribution of the DMTRP gene in various metazoans, including sponges, protostomes, and deuterostomes, indicates that it originated early in metazoan evolution. However, the DMTRP gene is only retained in marine species, and its loss seems to have occurred independently in ecdysozoan and vertebrate lineages from which major freshwater and land animals appeared. DMTRP may be an evolutionary and ecological limitation, restricting organisms that possess it to marine habitats, whereas its loss may have allowed other organisms to invade freshwater and terrestrial habitats.

Highlights

Utilization and regulation of metals from seawater by marine organisms are important physiological processes
In this study, we focused on the divalent metal transporter (DMT), which is called natural resistanceassociated macrophage protein 2 (Nramp2), a member of the SLC11 family, comprising proton-coupled metal ion transporters[10,11]
Alignment results of the scallop DMT with ApDMT and ApDMTRP are shown in Fig. S1. cDNAs of the two genes were cloned from starfish stomach because the fragments per kilobase per million reads mapped

Summary

Introduction

Utilization and regulation of metals from seawater by marine organisms are important physiological processes. Functional analysis using a yeast expression system demonstrated that DMT transports various metals, like known DMTs, but DMTRP does not. Based on the sequences detected, we cloned two different cDNAs encoding DMT-like proteins, one of which is an ortholog of known DMTs, but the other encodes an unknown membrane protein specific to marine invertebrates. We further analyzed their functions using a yeast expression system, and found that the unknown protein is quite unlike known DMTs. we will discuss the possible significance of this protein gene relative to the habitat transition of animals from the sea to freshwater and land

Methods

Results

Conclusion