Sclerite formation in the hydrothermal-vent “scaly-foot” gastropod—possible control of iron sulfide biomineralization by the animal

Abstract

A gastropod from a deep-sea hydrothermal field at the Rodriguez triple junction, Indian Ocean, has scale-shaped structures, called sclerites, mineralized with iron sulfides on its foot. No other organisms are known to produce a skeleton consisting of iron sulfides. To investigate whether iron sulfide mineralization is mediated by the gastropod for the function of the sclerites, we performed a detailed physical and chemical characterization. Nanostructural characterization of the iron sulfide sclerites reveals that the iron sulfide minerals pyrite (FeS 2 ) and greigite (Fe 3 S 4 ) form with unique crystal habits inside and outside of the organic matrix, respectively. The magnetic properties of the sclerites, which are mostly consistent with those predicted from their nanostructual features, are not optimized for magnetoreception and instead support use of the magnetic minerals as structural elements. The mechanical performance of the sclerites is superior to that of other biominerals used in the vent environment for predation as well as protection from predation. These characteristics, as well as the co-occurrence of brachyuran crabs, support the inference that the mineralization of iron sulfides might be controlled by the gastropod to harden the sclerites for protection from predators. Sulfur and iron isotopic analyses indicate that sulfur and iron in the sclerites originate from hydrothermal fluids rather than from bacterial metabolites, and that iron supply is unlikely to be regulated by the gastropod for iron sulfide mineralization. We propose that the gastropod may control iron sulfide mineralization by modulating the internal concentrations of reduced sulfur compounds.

Structure and mechanical properties of selected protective systems in marine organisms

“…Though uncommon, iron sulfide (FeS) is found within deep sea organisms: commonly bacteria, tube worms and a few gastropods, where the FeS is made available by deep sea vents [91,92]. It is often deposited on or absorbed into organisms and incorporated into their dermis to create an outer FeS shell [92].…”

“…It is often deposited on or absorbed into organisms and incorporated into their dermis to create an outer FeS shell [92].…”

“…An example is the deep sea scaly-foot gastropod Crysomallon squamiferum (Fig. 11), which employs an outer layer of FeS and a calcified inner layer that are separated by a relatively thick organic layer [92,109,110]. FeS is deposited on the surface of the mollusk by the deep sea vents in its natural habitat and incorporated into its structure [92,110].…”

“…11), which employs an outer layer of FeS and a calcified inner layer that are separated by a relatively thick organic layer [92,109,110]. FeS is deposited on the surface of the mollusk by the deep sea vents in its natural habitat and incorporated into its structure [92,110]. These FeS deposits are referred to as "sclerites," or elements of deposited mineral that are held together by a matrix (in this case the thick organic layer) in order to form a protective coating [92].…”

Renewable chitin from marine sponge as a thermostable biological template for hydrothermal synthesis of hematite nanospheres using principles of extreme biomimetics

“…These biomimetic principles also serve as a milestone in the development of new generation hybrid biocomposites. Nature exhibits numerous examples indicating biomineralization may take place under extreme temperatures (psychrophilic, or thermotolerant organisms [10]), pH and toxic metals (hydrothermal vent fauna [11][12][13]), and pressure (hadal deep-sea zone fauna) conditions. One of the basic points of Extreme Biomimetics is to find biomacromolecules possessing high chemical and thermal stability that are associated with mineral phase formation.…”