Astrobiology Revealed #21: Shuya Tan
on why microbes might be metal-starved in Enceladus’ ocean
by Aubrey Zerkle
In this Q&A, we asked Shuya Tan about his recent paper “Metal Limiting Habitability in Enceladus? Availability of Trace Metals for Methanogenic Life in Hydrothermal Fluids.” Shuya is currently a Young Research Fellow in the Institute for Extra-cutting-edge Science and Technology Avant-garde Research (X-star) at the Japan Agency for Marine-Earth Science and Technology (JAMSTEC). Shuya explains why scientists think methanogens could thrive in Enceladus’ ocean, and explores whether they’d have enough bioactive metals to do so.
How did you become interested in icy moon research?
I was first fascinated by the extreme landscapes and environments of icy moons during my undergraduate and masters courses. When I was a student, there were only a few institutions in Japan that conducted research on icy moons. In such a situation, I spent a part of my PhD at the Earth-Life Science Institute (ELSI) in Tokyo as a visiting student. During that time, I studied the ocean chemistry of Europa, the Jovian moon.
In your recent paper in JGR Planets you explored the potential for methanogens to live in Enceladus’ ocean. Why do scientists think methanogens in particular are likely to inhabit Enceladus?
In water plumes erupting from the surface of Enceladus, putative hydrogen and carbon dioxide have been observed by the Cassini spacecraft. These two compounds can be used as energy sources for hydrogenotrophic methanogenesis.
Other types of microbes are also possible in Enceladus’ ocean. For instance, methane oxidation has been suggested as another metabolic pathway, since methane itself has been detected in water plumes from there. In addition, iron-reducing or iron-oxidizing microbes have recently been considered as candidates. These microbes could use dissolved iron or iron contained in minerals, such as iron (hydro)oxides and iron sulfides, as energy sources. However, methanogenesis is considered the primary metabolic pathway, as electron acceptors in other pathways, like sulfate or oxygen, would not be abundant in Enceladus’ ocean.
You mentioned that Enceladus’ ocean has leftover energy and nutrients that we wouldn’t expect to see if life were thriving there. Earth’s oceans also have some areas with excess nutrients, e.g., the so-called high-nutrient, low-chlorophyll areas like the southern ocean. Could Enceladus’ oceans be similarly heterogeneous?
Heterogeneous material distribution could be present in Enceladus’ ocean, possibly providing clues to potential biomasses. Some trace metals could be provided by hydrothermal reactions at high temperatures (>100 °C), as shown in our paper. Hydrogen would also be actively produced by such hydrothermal reactions. On the other hand, low-temperature reactions would be thermodynamically favored for phosphate dissolution. Thus, trace metals and hydrogen would be contained in hydrothermal fluids, whereas cold seawater would be rich in phosphate. If microbes depend on the availability of all these ingredients, including trace metals, biological activity may be restricted to areas where hydrothermal fluids and cold seawater mix.
As you pointed out, there is chemical heterogeneity in the Earth’s oceans. I guess that they could be an analogue to the ocean of Enceladus. A lack of iron and other metals is also suggested as one of the potential factors limiting bioactivity in the high-nutrient, low-chlorophyll areas of Earth’s oceans.
You set out to test whether trace metals like Co, Ni, Cu, Zn, and Mo, rather than energy or macronutrients, could limit methanogens in Enceladus’ ocean. Why did you choose these specific metals?
These transition metals are utilized by life, including animals and primitive microbes on Earth. In particular, these metals are known as cofactors of enzymes and coenzymes in microbes, such as methanogens. Depression of bioactivity has been observed in previous cultivation experiments with methanogens [limited in these metals]. Such micronutrients are also industrially attracting attention since their addition improves the performance of anaerobic digestion of biodegradable waste. Thus, the habitability of microbes could be more strictly constrained by the availability of trace metals.
Although these metals are transported into the Earth’s oceans by terrestrial weathering on continents and aeolian dust, water-rock interactions on the seafloor or subseafloor would be their primary sources on Enceladus, with no continents and atmosphere.
Shuya thinks frozen lakes, like the one he’s sitting on here, could be similar to icy moons.
To test this, you calculated concentrations of metals in Enceladus’ ocean based on hydrothermal experiments and thermodynamic calculations - what was the most challenging aspect of the study?
The most challenging points were the interpretation of experimental results and the application of calculations to the experiments. Few previous studies have considered trace metals in water chemistry on Solar System bodies, such as icy moons and Mars. This is because, although observational constraints are critical in planetary environmental studies, trace metals are often found in limited abundances or are below detection limits.
On the other hand, these metals have been investigated in hydrothermal environments and ore deposits. Minerals containing trace metals are also identified in carbonaceous chondrites, which are analogous to rocks on the seafloor of Enceladus. Therefore, to interpret mineral phases containing metals in the experiments and to compile reliable thermodynamic data for performing the chemical calculations, it was necessary to refer to a large number of mineralogical and geochemical studies in these research fields.
You calculated that Ni, Zn, and Mo concentrations should be similar to Earth’s oceans, but Co and Cu could be low enough to limit methanogens. So is this a nail in the coffin, so to speak, for life on Enceladus?
At present, there are three possibilities for relations between life and trace metals in Enceladus. The first possibility is that microbial activity is limited by a lack of trace metals. Cobalt is contained in methyltransferase, which is the enzyme required for the conversion of carbon dioxide into organic compounds. Thus, a lack of cobalt could be a limiting factor for various types of methanogens and acetogens.
The second possibility is that life uses other metals instead of insoluble ones. For instance, iron and nickel are relatively soluble and are used by some microbes as cofactors in their enzymes, suggesting that they could potentially fill the gaps of insoluble metals. In this case, the variety of metabolic reactions would be limited, as the number of metal species that life can utilize is restricted. Thus, this case may also fall under the category where life activities are restricted.
The third possibility is that life may be independent of metal availability in the ocean. This is also not impossible. In a broader sense, microbes can acquire trace metals directly from the surface of rocks rather than from dissolved forms in the water [e.g., by using organic acids or molecules like siderophores to pull them out]. In this case, life would thrive in rocks on the seafloor or subseafloor, rather than in the oceanic water. In the future, we would like to explore whether any of these possibilities are realistic from a broad perspective.
Is there anything else you’d like to add that I haven’t asked you about?
This is a somewhat general topic. As an early-career researcher, I sometimes wonder if it is better to become an all-rounder who can do many things or a researcher with a strong specialty. Astrobiology has a wide range of diversity in both methods and objects. I have studied the inorganic chemistry of icy moons using multiple methodologies (e.g., laboratory experiments, numerical calculations, and surveys of analogue field sites). Although I have recently been trying to expand my scope, including organic chemistry and biology, I also feel the need to deepen my expertise. This may be a common concern among young researchers in the field of astrobiology.
Also, observability is important when considering habitability in the solar system. However, there is a possibility that observation is too difficult to provide sufficient evidence. To take an extreme example, explorations of the seafloors of Europa or Enceladus are almost impossible. I suppose that we need to consider how realistic research can be conducted for the habitability of such planetary objects and environments.