Astrobiology Revealed #4: Roy Price

by Aubrey Zerkle

In this segment, we spoke with Roy Price, Assistant Professor in the School of Marine and Atmospheric Sciences (SoMAS) at Stony Brook University. In his recent paper, “Quantifying the bioavailable energy in an ancient hydrothermal vent on Mars and a modern Earth-based analogue”, Roy and colleagues explored shallow hydrothermal vents in Iceland to imagine what types of microbes might have lived in similar environments on past Mars. Roy talks about his path from arsenic to Eridania, Scuba diving around the world, and why oxygen is an analogue scientist’s worst nightmare. (This interview has been edited for length and clarity.)

How did you go from a PhD on arsenic cycling and groundwater contamination to studying hydrothermal vents on Mars?

Well, I've always been fascinated with astrobiology, and the arsenic stuff took me in that direction on its own. I'm sort of an armchair microbiologist and astrobiologist, I love reading about physics and astronomy. I've always loved biology, but I was really good at chemistry, so I went down that route instead. But I always loved it, everything I learned about it I always tried to learn more.

The connection was really through my PhD work in Papua New Guinea, which was a National Science Foundation funded Biocomplexity project. That was a big project, and it had four professors who each had a PhD student. The PI was my advisor, and one of the Co-Is was Jan Amend, who is a microbiologist. He does something I really like, which is bridging the gap between microbiology and redox chemistry using Gibbs Free Energy thermodynamic calculations.

My interest in shallow sea hydrothermal vents was an aside from the arsenic work. There were high concentrations of arsenic in the shallow sea vents from volcanic systems that I was studying. Then, in the early 2000s I saw a paper from Deb Kelley and others about the Lost City Hydrothermal vent field, and I was immediately fascinated, blown away, and wondered could these perhaps occur in a shallow sea environment.  

And so I started looking [for shallow sea hydrothermal vents]. I didn't look in the scientific literature, because I would have known if any were described there. Where I looked was on Scuba diving websites. For studying shallow sea vents we don't use ROVs, and sometimes we don't even use ships. We can go Scuba diving from the beach or from a small boat. So, if there was a site like the Lost City in a shallow environment, there would probably be Scuba diving happening on it, from a commercial point of view. 

I found two sites. One was in Iceland, the Strytan hydrothermal system, which this paper is about, and the other was in New Caledonia in the South Pacific, called the Prony Bay hydrothermal field. I’ve since had a chance to work on both of those. I've been to both sites 4 or 5 times, I've been very lucky. When I looked in the literature, the Strytan site had only one paper about it. This was in 2001, which was exactly the same time as the Lost City paper came out. But that was it, and I was like “Oh wow, what an opportunity!”

A photo of the Strytan hydrothermal field from your paper made the cover of the April issue of Astrobiology - it looks incredible! Can you tell us why that environment is so relevant to Mars?

Yes, for a couple of reasons. First of all, Iceland’s geology is such that the rocks are made of basalt [like the rocks on Mars]. And so, whenever you have water-rock reactions with basalt, it is analogous to early Mars, when Mars had a lot more water than it does now.

 [The second reason is that at Strytan] you also have a hydrothermal system that’s groundwater-sourced and precipitating out massive saponite [a type of magnesium silicate mineral produced by low-temperature reactions between water and mafic minerals]. It was a 2017 paper from Joe Michalski describing the Eridania Basin on Mars that allowed me to put two and two together and say the Strytan system is an analogue for the Eridania Basin. He had this cross-section in the paper that showed rain falling on land, then groundwater percolating through basalt and coming out into the basin. And that cross section looked almost exactly like one I had drawn for Eyjafjord, which is where the Strytan system is. You put them side by side and they look just alike, they have rainwater-fed groundwater, and they have saponite in them, and the same kind of hydrothermal discharge of silica-rich fluids into the basin. In Eridania Basin on Mars the saponite is massive, on the level of a Great Salt Lake or something like that, giant amounts of saponite. Some would argue Eridania Basin wasn’t a hydrothermal system like Iceland, it’s up for debate. But if it does have hydrothermally-precipitated saponite, that’s a very interesting aspect that connects the two systems.

So I wrote a NASA Habitable Worlds proposal to study the habitability of Eridania Basin on Mars through the lens of the Earth analogue of Strytan. The way we did that was to get the chemistry of Strytan, model the chemistry of what would have happened in Eridania, and then do bioenergetics calculations based on the Gibbs Free Energy. These calculations allow us to get a sense of, if there were microbes there, was there an energetic drive for them to support their lives through some redox chemical reactions.

You mentioned that you went to Scuba diving websites to look for shallow sea hydrothermal sites. Are you a driver? Did you do the fieldwork yourself? 

I did, yes. I’ve been extremely lucky! I’ve been Scuba diving for science all around the world, in the Mediterranean, the South Pacific, the Caribbean, Iceland, and many other places. Of course I try to make that happen as much as I possibly can because I love to Scuba dive as well. 

I started Scuba diving when I moved to Florida. After I had finished my bachelor’s degree in geology and started a master’s degree in hydrogeology [at the University of South Florida], I was Scuba diving recreationally for fun. And then I started my PhD with my advisor Thomas Pichler, who’s in Germany now. He was a Scuba diver, and his focus was shallow sea hydrothermal vents. Around the time I was finishing my master’s degree he got this Biocomplexity grant funded and he immediately asked me if I wanted to do my PhD with him, and I said yes. Then I spent four more years Scuba diving there, and in Mexico, and Dominica, and the Caribbean, and other places. Ironically, that was the arsenic story. Arsenic was coming out of the vents – we wanted to know where does it go, do the coral reef reef organisms take it into their tissues, and what happens to it then. 

Then I decided I wanted to do something different, and I got this postdoc here in Germany at the MARUM Center for Marine Environmental Sciences at the University of Bremen. I had my own funding, so I went to the Mediterranean, to Greece, and I was island-hopping around these places that had shallow-sea hydrothermal vents. I collected some samples around the island of Milos in Greece, where I recorded the highest arsenic concentration of any hydrothermal vent in the ocean. It was orders of magnitude higher than black smokers or anything like that, so I spent the next three or four years working on the arsenic story there again.

Only then, after I got my second postdoc with Jan Amend, did I start working on the Lost City analogues and start applying for funding from NASA and things like that. 

It’s always exciting to hear the kinds of awesome opportunities that can develop from analogue projects like this! You explained you used thermodynamic calculations to model the metabolisms of microbes in the hydrothermal systems. What’s the biggest uncertainty in these types of models?

Any model inherently has some uncertainty involved. Basically, there are two avenues you can go for a comprehensive thermodynamic assessment of the habitability [of an environment]. One is focused on the chemotrophic microbial activity, so those would just be redox reactions. For example, imagine sulfide reacting with oxygen, creating sulfate. That chemical equation has an inherent thermodynamic drive to proceed in one direction or the other. [The Gibbs Free Energy calculations compute that drive.] The other avenue is heterotrophic reactions [microbes that use carbon compounds in their metabolisms], and that’s something I’m working on right now. Our paper that’s in Astrobiology is just about the inorganic reactions, so it's really only half the story.

There are also inherent uncertainties involved in the assumptions that we make when we do those calculations. Typically, they're not done at standard temperature and pressure. We’re dealing with hydrothermal fluids, so the temperatures are higher, and in fact we're targeting environments that we cannot sample directly. That's particularly true for the Mars side of the story. Three to 4 billion years ago, when Mars was an ocean world, we have only a vague idea of what the atmospheric composition would have been, much less the groundwater chemistry reacting with the basalt or the basin fluid. So that had a lot of inherent uncertainties with it. The Iceland system had far fewer assumptions, and therefore we can be a lot more confident in the results. There you just go Scuba diving, you measure the chemistry, and then you do the calculations. It's really quite straightforward.

How did you go about recreating the chemistry of ancient hydrothermal systems on Mars?

For Mars, we had to first figure out what the atmospheric composition was 4 billion years ago. We then reacted that with pure water, to make a rainwater that had dissolved gases in it. Then we rained that water on this 4 billion-year-old basalt. The basalt compositions were not directly from the Eridania basin environment, they were actually from Gusev crater. That's a long way north. Geologically speaking, it's far removed not only in time but in space, so we are assuming that the rock types were similar in the same environment. We have a vague idea through the CRISM orbiter data that they're kind of the same thing. Then we reacted that atmospherically-derived rainwater that became groundwater with those basalt compositions and created our own hydrothermal fluid. So we made, or modeled, a 4 billion-year-old hydrothermal fluid on ancient Mars. And that’s pretty cool!

Then, there was an older paper by Catling, who had thought about what the [Martian] basin compositions would have been, based on evaporite deposits. [Which was important because] we not only needed the discharging hydrothermal fluid, we needed to mix it with the basin fluid as well. So we used those basin fluid compositions estimated from evaporites, reacted it with the hydrothermal fluids we modeled, and did the bioenergetic calculations for the inorganic redox reactions. And we came up with this story that the microbial activity on early Mars could have been methanogenesis, but that methanogenesis would potentially have been very different from what it was like on early Earth because of the higher nitrogen concentrations.

Why are the microbial metabolisms predicted by your models so different from what we currently see anywhere on Earth?

Now, therein lies our biggest uncertainty. Our reactions were basically CO2 or bicarbonate reacting with nitrogen species, like ammonium or N2, creating nitrate or some other nitrogen species and methane. That has never been recorded as a microbial metabolism on Earth. Can it happen on Earth? It potentially could, if the microbes have the genetic capabilities. We haven't recorded that either. It doesn't mean it has never existed, though. Maybe it existed on the early Earth and microbes have evolved to have much easier metabolisms, energetically speaking.

That’s strange, right. Why would you have that? We started looking at it, and the atmospheric compositions that we assumed were from two papers that were focused on seeing if there were enough greenhouse gases in the atmosphere to create liquid water on early Mars. Using that atmospheric composition, which we wanted because we wanted liquid water, there's a lot more nitrogen in the atmosphere, and that led to having high nitrogen in our rainwater.

When nitrogen gets reduced in the hydrothermal system it becomes ammonium, so that is a huge driver of that bioenergetic capability. If you take away that nitrogen, you would be left with basically hydrogenotrophic methanogenesis. I think a lot of people would argue that is a more viable microbial reaction. If we tweaked our atmospheric composition assumptions a little bit, hydrogenotrophic methanogenesis would be the primary reaction [in the Martian hydrothermal system]. And I talk about that in the paper.

You have a sentence in your paper that I think really resonates beyond this particular study, which is “The likelihood of these catabolisms can only be evaluated in context of Earth microbiology.” How big an obstacle do you think Earth bias is for astrobiology in general? 

Oh, it’s a huge problem, and a huge bias. But we're stuck with it. There's not much we can do! I think there are other people who have a much better sense of that than I do. I think Mike Russel was probably the person who said that “life contaminates”. Basically, there's no way to get away from it.

In our system in Iceland, for example, what we found is that most of [the microbial reactions] were driven by oxygen. Early Mars and early Earth would’ve been devoid of oxygen for the most part. So most of the hydrothermal vent research that we look at today in the context of origin of life or astrobiology is biased by the production of oxygen by life on Earth. That's a real issue and a real problem. 

We have a paper that came out last year describing the microbial ecology of the Strytan vents. The bacterial strains dominant there are Thermocrinis species and Thermus species, and those are microaerophiles, even though the fluids coming out are anaerobic. As far as we can tell, there's just a little bit of oxygen from seawater mixing throughout the whole edifice, which is huge, it's 55 meters tall. It's unbelievably big! But [that small amount of oxygen] is driving the microbial communities there.

Right at the vent tips where the water is coming out, those microbes are microaerophiles. They’re not strict anaerobes, which is fascinating to me! Saying this is the best analogue ever for an Eridania Basin early Mars then becomes a challenge because of the oxygen. Yes, [the Strytam system] is precipitating massive saponites, but it's contaminated by life through the abundance of oxygen. 

So how do you solve the problem of oxygen contamination on modern Earth?

Well, one thing I'm writing a proposal about right now is [asking the question], how do we find an environment that’s a better analogue [for Martian hydrothermal systems]? In the subsurface in Iceland, there are wells with water that doesn’t mix with seawater. The oxygen that we see at Strytan is coming from seawater. But in the northern part of Iceland, that’s a hot aquifer, a groundwater system that’s heated by proximity to the spreading ridge, so the wells are anoxic. The rainwater has more CO2 and more oxygen in it [than on early Mars], but that oxygen is quickly consumed by microbes within meters of the groundwater recharge zone.

These aquifer systems are traveling long distances underground, through lava, getting heated up, with no oxygen, and then all over Iceland they drill holes and get geothermal energy for electricity and things like that. The proposal I'm writing is really focused on trying to access that environment, to understand the microbiology there, as more of an analogue to early Earth and early Mars environments devoid of oxygen. 

And that leads into my next question, which is, what do you plan to do next with this research?

There are two directions. [The first one is] organics and heterotrophic metabolisms, that’s an ongoing struggle, but we’re working on it. That part of the project was a lot more challenging than I anticipated it would be, because you need to have concentrations of organic compounds in your fluids and all the reactants. And to do a comprehensive evaluation of all the different types of organic compounds there, that’s a challenging analytical problem. And I think we’re getting there.

The other one is to find environments, natural or synthetic, where we can control the oxygen, and then try to understand how the microbes respond to oxygen. Have you seen anything about our mini-cones, these artificial cones that we’re growing in Iceland?

No, I haven’t heard about that. What are mini-cones?

I realized the groundwater feeding the Strytan system is the same as what comes out of the hot water taps. People in Iceland fill up their hot tubs with hydrothermal fluid from the taps. So in Northern Iceland where the Strytan cones are, we can just turn on the tap and have access to the end-member hydrothermal fluids from a well. In Strytan, mixing of silica-rich hydrothermal fluids with magnesium-rich seawater builds these massive cones of saponite, which is magnesium silicate. So we did some experiments where we took some of the hot water from the tap and mixed it with seawater, and all of the sudden we had precipitates! 

That’s a really cool part of the story and part of the next steps as well, where we can manipulate a system that's kind of a natural system but it's artificially made. The dive shop in Northern Iceland is an old halibut nursery and herring fishery. It’s a huge building, and they have these two meter by two meter by one meter deep tanks, where they can flow through fresh seawater. So I took a hose and put it into that pool and built my own Strytan cones by running hot water from the tap into it.

[The artificial mini-cones] grow 6 to 10 centimeters tall, and have saponite, Thermocrinis, the whole thing. It's an artificial, natural system. So that’s part of the next steps as well, to play around with that system and manipulate it so that we can see the interactions of oxygen, and how that affects the microbial communities. (See Roy’s real-time mini-cone cam on YouTube!)

Is there anything else that you’d like to mention that I haven’t asked about? Like any advice for early career astrobiologists?

You know, it's a team effort. You must give a shout-out to my co-authors. In particular, Holly Rucker is the lead author of this paper. She was a master’s student with me, she's now a PhD student. She did most of that work. The ideas were mine, but she really brought it home, and so I can't say enough about how good she is. She’s got a good career in front of her.

I relied heavily for this paper not only on Holly, but on Doug LaRowe who helped Holly with all the energetics calculations. I can do them, but I’m not an expert. [Doug] is one of the world’s experts, so he did an amazing job. For the water-rock reactions and all the modeling on Mars, Tucker Ely did that. That was using EQ6, which we talk about in the paper, but that's not something I'm an expert in either. I can do a little bit of Geochemist’s Workbench stuff, but I couldn’t have done this paper without their help.

And I think that's it – it takes a team, it takes interdisciplinary work. If you have an idea but you don't know how to make it work, talk to people and try to collaborate. Hopefully it’s someone you can trust, and that you develop a good relationship with, and you can move forward from there. So that's one thing, it's really important to build a network and build collaborations as soon as you can if you're an early career scientist!