Chrysomallon squamiferum:

The water column in the ocean can be divided into zones based on the available light levels. The top 200m of the water column is the euphotic zone, in which there is enough sunlight for photosynthesis to occur. From 200m to 1000m is the dysphotic zone, in which there is not enough sunlight for photosynthesis but just enough that some organisms, often with large, modified eyes, can see. Below 1000m is the aphotic zone, which no sunlight reaches at all.

All animals are heterotrophs, meaning they cannot simply ingest inorganic carbon (CO₂) and turn it into organic molecules, like glucose, necessary for bodily functions. Instead, they must rely on (i.e. eat) the carbon fixed by primary producers, which are organisms that can convert CO₂ into organic molecules.

The vast majority of the organic carbon in the ocean is fixed in the euphotic zone by photoautotrophs like algae and phytoplankton, and travels through the food web to the largest of predators (including us humans, when we enjoy a shrimp cocktail or a tuna sandwich).

As we dive deeper into the water column, the amount of available organic carbon shrinks dramatically. Most of the organic carbon fixed in the euphotic zone is consumed in the euphotic and dysphotic zones, and, in fact, less than 1% of the total carbon fixed in the euphotic zone actually reaches the ocean bottom! This makes the benthos—the ocean floor—an extremely food-starved habitat. So how does the scaly-foot snail make do on the benthos?

The answer is symbiosis with chemoautotrophs! The scaly-foot snail hosts, within the cells of its esophagus, bacteria which can fix CO₂ into organic molecules by harnessing the energy from the oxidation of sulfur, abundant in the plumes of hydrothermal vents, rather than sunlight in a process called chemosynthesis.

In exchange for safety from grazers and a guaranteed supply of raw materials in the comfort of the scaly-foot snail’s cells, the bacteria provide sugars, amino acids, and vitamins that the scaly-foot snail cannot produce on its own (Lan et al. 2021), in addition to the disulfide anion needed for the iron sulfide layer of the snail’s shell and sclerites.

A mid-ocean ridge is a seafloor mountain system where magma rises through a crack in the oceanic crust and hardens into dense basalt. Over geologic time, the creation of new oceanic crust at the mid-ocean ridge displaces existing oceanic crust, contributing to plate tectonics.

The Indian Ocean, where the scaly-foot snail is found, is criss-crossed with four mid-ocean ridges: the Carlsberg Ridge, Central Indian Ridge, the South West Indian Ridge, and the South East Indian Ridge.

As seawater percolates into the rock at a mid-ocean ridge, it is heated by the magma below, picks up dissolved minerals like iron, copper, and sulfur, and is expelled in a thick black plume through a hydrothermal vent. The mineral-rich vent plumes sustain chemoautotrophs like the endosymbiotic bacteria of the scaly-foot snail. The Indian Ocean hosts 13 confirmed hydrothermal vents (van der Most et al. 2021).

Scaly-foot snails were first discovered in the Kairei vent field at the Rodrigues Triple Junction in 2001 (Van Dover et al. 2001). Another population was discovered farther north in 2009 at the Solitaire vent field (Nakamura et al. 2012), and to the southwest on the Longqi vent field in 2011 (Chen et al. 2015). This means that only three populations of the scaly-foot snail are known.

The Solitaire vent population is remarkable in that it does not have the typical black iron sulfide armor found at the Kairei and Longqi vents. The absence of an iron sulfide layer is likely due to the fact that the iron concentration at the Solitaire vent field is only 60μM—while it is still double the average iron concentration of the sub-equatorial Indian Ocean (27μM; Chinni et al. 2019), it is still only 1/58th of the concentration at Kairei vent field (Okada et al. 2019)!

Despite the significantly different appearance of the Solitaire population, genetic studies show that the Kairei and Solitaire populations are genetically indistinct from each other (p = 0.576) but significantly different (p < 0.001) from the far-off Longqi population (Chen et al. 2015). This implies that the scaly-foot snail has a limited dispersal range, further supported by evidence that the scaly-foot snail’s eggs are negatively buoyant (Beedessee 2013), preventing larva from floating long distances to colonize new vents.

This is significant because China and Germany have been granted exploratory licenses to investigate mining Longqi and Kairei vent fields, respectively, for massive sulfide deposits by the U.N. International Seabed Authority. If the Longqi vent population were to be wiped out by the destruction of hydrothermal vents, it is unlikely that larva from other populations could resettle the vent field once the vent stacks recovered (if at all), and the genetic differences may hamper their survival. And the eradication of the Kairei vent population would effectively halve the eastern range of the scaly foot snail. The scaly-foot snail was officially registered as an Endangered Species in 2018 after a successful lobbying effort by Julia Sigwart and Chong Chen, two scientists studying the scaly-foot snail (Sigwart & Chen 2018).

In the last two decades, much of the attention on the scaly-foot snail has been focused on its unique biomineralization.

From studying its anatomy, we now know that it is the only known animal to carry out biomineralization with sulfur, rather than oxygen, and that it carries out such biomineralization by extruding, through microscopic channels, streams of disulfide anions to bind with iron cations to form a layer of iron sulfide on the outside (Okada et al. 2019).

From studying the ecology of the scaly-foot snail, we know that the disulfide anions are produced as byproducts of chemosynthesis from endosymbiotic bacteria (Lan et al. 2021).

Finally, from studying the populations of the scaly-foot snail, we know that environmental concentrations of iron is important. In iron-poor environments like the Solitaire vent field, the scaly-foot snail will not create iron sulfides at all, while the genetically indistinct Kairei population easily creates a layer (Nakamura et al. 2009).

What is still unknown is whether the iron cations come directly from the diffuse flows around the hydrothermal vent, or if it is biologically mediated. Goffredi et al. (2004) suggest that, owing to the abundance of certain types of bacteria on the surface of the sclerites that bacteria mediate the provision of iron cations; Okada et al. (2019) instead offer that the disulfide ions directly come in direct contact with iron cations in the diffuse flow.

This is a small but important step in the synthesis of iron sulfide because, currently, no cost-effective method of synthesizing metal sulfide nanoparticles exists (Yamashita et al. 2023). A method allied with bacteria could potentially be the solution to a cheaper manufacture of solar panels.

The question of whether iron cations are provided passively by the vent plume or actively mediated by bacteria can be answered by comparing iron isotope fractionation patterns—the maintained ratio of iron isotopes—of the surface bacteria, the vent plume, and the iron sulfide layer of the shell and sclerites.

Organisms, especially bacteria, tend to modulate the isotopic ratios in its metabolites (e.g. Kappler et al. 2010), and hydrothermal vents tend to vary in isotope composition even within the same vent field (Nasemann et al. 2018). Therefore, if the iron isotope fractionation of the iron sulfide layer agrees the bacterial iron isotope fractionation and disagrees with the vent plume iron isotope fractionation, then we have evidence to conclude that the introduction of iron cations involves biological mediation in the form of bacteria. A detailed experiment plan is available here.

Yet other unknowns exist, including what the complete life cycle of the scaly-foot snail looks like—we do not know what its larval stages look like, nor how it spread from vent to vent in the first place, though we know that its range is quite limited following genetic studies. Further, we do not know how sensitive it is to temperature, given that it must stay within a narrow range of plume water to feed its endosymbionts, and how environmental toxins, like ones released by deep-sea mining, affect it, given its prodigious circulatory system.

These open questions all require prolonged in situ observation, collection, and documentation, which is made difficult by the fact that HOV and ROV dives are time-limited and contingent on weather conditions. All the more reason to protect the scaly-foot snail until we can answer all these questions... then come up with even more questions!