The making of natural iron sulfide nanoparticles in a hot vent snail

Abstract

Biomineralization in animals exclusively features oxygen-based minerals with a single exception of the scaly-foot gastropod Chrysomallon squamiferum, the only metazoan with an iron sulfide skeleton. This unique snail inhabits deep-sea hot vents and possesses scales infused with iron sulfide nanoparticles, including pyrite, giving it a characteristic metallic black sheen. Since the scaly-foot is capable of making iron sulfide nanoparticles in its natural habitat at a relatively low temperature (∼15 °C) and in a chemically dynamic vent environment, elucidating its biomineralization pathways is expected to have significant industrial applications for the production of metal chalcogenide nanoparticles. Nevertheless, this biomineralization has remained a mystery for decades since the snail's discovery, except that it requires the environment to be rich in iron, with a white population lacking in iron sulfide known from a naturally iron-poor locality. Here, we reveal a biologically controlled mineralization mechanism employed by the scaly-foot snail to achieve this nanoparticle biomineralization, through δ34 S measurements and detailed electron-microscopic investigations of both natural scales and scales from the white population artificially incubated in an iron-rich environment. We show that the scaly-foot snail mediates biomineralization in its scales by supplying sulfur through channel-like columns in which reaction with iron ions diffusing inward from the surrounding vent fluid mineralizes iron sulfides.