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Down the Rabbit Hole: Exploring The Deep Sea – Peter Girguis, Harvard University

Peter Girguis is a Professor in the Department of Organismic and Evolutionary Biology at Harvard University. Peter’s research explores extreme environments and the lives and behaviours of the organisms who live in the deep sea. In this interview, Peter discusses bioluminescence, ocean-dweller metabolisms and how using genomic, transcriptomic and proteomic techniques can help us understand the largest habitat on our planet.

Please note the transcript has been edited for brevity and clarity.

FLG: Welcome to the latest ’Down the Rabbit Hole’ interview. Today, we’re going to be talking about extreme environments and the deep sea. I’m joined by Peter Girguis. Pete, could you please introduce yourself and tell everyone a little about what you do?

Peter Girguis: Thank you for the invitation. My name is Pete Girguis. I’m a professor at Harvard University in the Department of Organismic and Evolutionary Biology. The research that we do focuses on understanding how organisms, animals and microbes have evolved to make a living in the deep sea. Much of what we do is through the lens of genomics, transcriptomics and proteomics. But, I’m also a physiologist at heart and began my professional career as an animal comparative physiologist, which means we’re really interested in understanding performance. How do animals work? What’s their metabolic rate? So too for microbes. What are their metabolic rates? How much energy are they harvesting? How much power do they generate? And how does that shape their fitness and change the world around them? We’re an integrative lab and we cross-cut physiology, ecology and evolution.

FLG: Before we get down to the molecular, let’s start more broadly. Can you define what counts as an extreme environment? What actually counts as the deep sea?

Peter Girguis: Poppy, this is one of my favourite questions, because what an extreme environment is, depends on your point of view. When we as humans talk about extreme environments, what we’re really talking about are environments that are extreme for us. The desert may be an extreme environment because it has little water and higher temperatures. We view the deep sea as an extreme environment and the deep sea has extremes. There is a lot of nutrient limitation throughout most of the deep sea, because it is dependent on the plant and algal productivity in the upper ocean that settles down into the deep sea. It’s kind of like being at the tail end of a queue, in a buffet line, and by the time you get to the buffet, the stuff that few people want is all that’s left. So too in most of the deep sea. In that sense, it’s kind of extreme. Nutrient limitation is an extreme condition.

There are other places in the deep sea, like hydrothermal vents, that really are extreme when you think about our biosphere. They are areas where you have microbes living at the hottest temperatures, in acidic fluids, and dealing with metals and other toxins. They really are at the edge of our biosphere.

But, when we say extreme, it is really from our point of view. I would point out that the deep sea itself is 80% of our planet’s living space. Any water that is below a kilometre and depths beyond the reach of sunlight is considered deep sea. If you look at it through that lens then, arguably, they are the normal ones, and we are much more extreme or in the minority. From the point of view of deep sea animals, we are the ones who somehow managed to make a living in this dry, arid environment.

FLG: That’s fascinating and the fact that it only starts a kilometre away – that’s only a 10-minute jog, depending on your running speed! So, it’s one of our largest habitats on the planet, but we know so little. What are some of the adaptations we are seeing in these marine organisms? You were talking about your interest in traits earlier, the behaviours, give me the weird and the wonderful.

Peter Girguis: You know what’s weird and wonderful about the deep sea? Let’s take a step back and talk about what it is. It is ocean that is a kilometre or deeper and is beyond the reach of sunlight. One of the most interesting things about the deep sea is that in many places there is plenty of light, but it is light made by other organisms. Bioluminescence is when organisms make their own light through a chemical reaction. Experts believe that it has evolved independently about 40 times. That underscores its importance to that environment. I have had the fortune of going on submersible dives, sitting in a tiny little submarine sinking three kilometres below the sea surface. As soon as you get down to where the sunlight begins to attenuate, it gets a little bit dark, it’s just an indescribable light show when you look out the window of the submersible. Bioluminescence is this incredible capacity that is found in so many different phyla. It has evolved independently so many times, so that’s one of my favourites. I don’t study bioluminescence per se, that doesn’t matter. I love seeing what people learn when they study how organisms make light.

Let me share one fun story about bioluminescence and then I’ll move on to some other really weird and wonderful things. There are fish that live in the deep sea that produce blue-green bioluminescent light. That is the normal colour of most bioluminescence and there are a lot of reasons for it. Those wavelengths travel well through water, and it is a way of communicating with one another. But there are some species of fish that have evolved the ability to produce and see red light. We believe they use it like a kind of night vision, so they can shine red light out from these little photophores, these light producing organs under their eyes, illuminating the area in front of them and most of their prey probably can’t see the red light. What an extraordinary adaptation! It’s like fish have come up with night vision well before humans ever did. It’s a wonderful example of just how natural selection works to produce these capacities that give these organisms a little edge in terms of their fitness.

It’s also neat to see how animals and microbes make a living with the little food that they do have. There’s that old adage, “One person’s junk is another person’s treasure,” and there are plenty of organisms in the deep sea that make a living off of eating faecal matter and fish scales. There are all sorts of amazing adaptations to deal with these sort of low nutrient, low food-quality diets. They are successful and they have been there for millennia. They have this capacity to hone in on foodstuffs and some of them are really specialised. For example, big mucus nets to catch fish poo as it rains down. Although the quality of the food is low, as long as you get enough of it, you’re fine. I often tell students and friends, you can meet your daily caloric requirements by eating a handful of candy bars, or a couple of bushels of celery. But, if celery is the only food around, and no one else wants it, there’s a solution. Those are two really fun and exciting adaptations in the deep sea, and we haven’t even talked about hydrothermal vents yet, which are their whole own amazing place.

FLG: I’m happy to go straight to the hydrothermal vents, and I’m assuming this will take us down to the small stuff, a lot of the bacteria and the microbiome down there as well. Let’s talk about the vents and your interdisciplinary work with the molecular biology you’re discovering there.

Peter Girguis: Vents are a bit near and dear to my heart, ever since I was an undergraduate. I started off my undergraduate life wanting to be an eye surgeon, but I disliked the classes. Also, ironically, I think there are minimum vision requirements for eye surgery, and I don’t meet them. So, I bailed on this idea of being a doctor and turned to Italian history in the Renaissance. I was very interested in the progress of science, not just in Europe, but around the world. Then, I took an oceanography class and was instantly hooked, especially because of vents.

Vents were discovered in the late 1970s, around about the time I was 10, and I remember reading about them as a young boy and thinking oh my goodness, underwater volcanoes and hot springs… how crazy is that? As an undergraduate, I was really fascinated by them, as I was studying marine science. I then went to graduate school to study the hydrothermal vent tubeworm, Riftia. This is the poster child of hydrothermal vents and many people have seen them. They are these large, one or two metre long, big red worms. Let me tell you about some of their adaptations, and then I’m going to move to the microbes which are really the star of the show.

Riftia is this mouthless gutless worm. It doesn’t have a mouth, a digestive tract or an anus. It is a worm that doesn’t eat food in the way we eat food, and this baffled people for a few years. They thought maybe it absorbed nutrients from the vent water and they thought it grew so big because they lived in the warm water around vents. The worms don’t live at really high temperatures; they like bathtub temperatures like you and I. Nobody really figured this out until two scientists independently started looking at the so-called ‘guts’ of the worm, the insides of the worm, and they found bacteria.

These bacteria are capable of harnessing energy from chemical reactions, similar to what you and I do. We take organic matter and oxygen, we react them, and we harness the energy from that reaction. Only they don’t use organic matter, they use hydrogen sulphide, and this is where things get really weird. The bacteria are capable of using hydrogen sulphide and oxygen, and hydrogen sulphide has got lots of electrons to give up. In fact, it’s flammable.

Hydrogen sulphide is that rotten egg smell that comes out of sewers, and believe it or not, at high enough concentrations, like those found at vents, it’s toxic to animals. This was mystery number one, these worms have these bacteria living deep inside them, symbiotically, that need hydrogen sulphide and oxygen. The worm is an animal like you and me, so how does it get sulphide to the symbiotes? Well, the worms have evolved haemoglobins that bind to oxygen, like you and me, but also bind sulphide and they deliver them to the bacteria. The bacteria carry out the reaction harnessing the energy and they fix carbon dioxide to sugars just like plants. But they do this in the darkness of the deep sea. A lot of my research as a graduate student focused on measuring the following metabolic rates: how much sulphide is taken up, how much oxygen is used, how much energy is available, and how much carbon is fixed. I had the real fortune of working on that, as well as building and developing one of the first life support systems for these deep sea animals. That’s the physiologist in me, studying metabolic rates.

Fast forward to my starting this lab at Harvard. I became very interested in the molecular underpinnings, wondering how does this work? Colleagues of mine had discovered evidence that these symbiotes fixed carbon, not just through one, but two different pathways. These are colleagues of mine in Germany, who did some excellent work with proteomics to show that there are proteins capable of fixing carbon with two pathways. This immediately caught my attention for two reasons. Believe it or not, this worm, with its symbiotes, are some of the fastest growing animals on the planet. Doing those metabolic rate measurements as a grad student meant that I could measure how fast they grow. They can fix 10% of their body carbon a day. This is stupefying! Imagine going to bed, weighing 100 kilogrammes, and then 110 the next day, and then 121 the day after that. It’s insane, but that’s what they do.

A lot of our work now is really focused on keeping these animals alive at the conditions they find at vents. We have built high pressure aquaria, high pressure pumps, and we use mass spectrometers to measure their metabolic rates. Then, via transcriptomics, proteomics and metabolomics, we look at the molecular mechanisms underpinning these extraordinary carbon fixation rates. That’s what our work is right now and we’re beginning to untangle how they use these two different carbon fixation systems. We couldn’t do that if we didn’t have the tools that we have now with transcriptomics and proteomics. What really excites me is that we can ally metabolic activity, function and the growth of this worm to these molecular processes, so that we have a kind of single-cell to animal to community perspective on how they function.

FLG: Knowing that these techniques are enabling us to see and learn so much more about these almost alien life forms that are so separate from our life on surface is so exciting. How does the circadian rhythm work for creatures deep down? Does it even exist?

Peter Girguis: That is a very good question. I don’t think there has been a huge amount of work done on circadian rhythms. We do, however, see periodicities in their metabolic rate. I have an interest in how animals shape the environment around them. We build a lot of geochemical sensors in my lab, underwater mass spectrometers that analyse the chemical environment around the worms, temperature probes that record changes in temperature over time. Through our temperature measurements, we are able to see what look like tidal pulses in fluid flow. This means, from the point of view of a worm, you see changes in temperature and chemistry. They experience a change that is quasi-tidal. I’m not a geophysicist, so I can’t explain this, but it does remind us that the moon is pretty big and actually influences fluid flows and other processes even down a couple kilometres.

FLG: That’s phenomenal. Diving back to the ocean microbes, what are we learning that might shape our lives above surface, whether that is to do with our own health or to do with ecosystems and climate?

Peter Girguis: Let’s start with the tubeworm symbiotes and then I’ll share a bit about some free-living microbes that we study through the lens of transcriptomics and proteomics. The worm’s symbiotes have two carbon fixation pathways and are fixing carbon at tremendous rates. There is an interest in thinking how we might use biological organisms, microbes, plants and algae to aid in carbon sequestration. These microbes, along with their tubeworm hosts, sustain phenomenal rates, some of the highest ever measured. They are fixing carbon at rates similar to what we see in the fastest growing algae and plants. Being able to do that in a bacterial culture, like a big fermenter, offers a lot of possibilities that you might not get without algae. Growing kelp forests to sequester carbon is great, but imagine being able to have a fermenter with microbes that can fix carbon as it comes out of a natural gas plant. So, there is this applied bent to the work.

We also study free living microbes that oxidize methane, and there’s an awful lot of methane in our world. Most of it is biogenic, meaning it is produced by microbes, most of it is in the deep sea and very little of it actually escapes the ocean. But my lab and many others have worked on these microbes that oxidize methane, both with oxygen and without, to ask whether we can use these organisms to sequester methane and produce a by-product? If they are harnessing energy for methane oxidation, could they produce a biofuel? Something that is less problematic than just the combustion of methane, and there are many pros and cons to these ideas.

But, in my lab, we really study these microbes that live at vents with an eye towards understanding their fundamental attributes. How do these microbes, for example, lay down the mineral pyrite? We have done research on microbes that deposit pyrite at hydrothermal vents, and pyrite is a semiconductor and can be used as solar cells. They are not as efficient as the ones today, but if you could figure out how to get microbes to grow a solar panel, that is a game changer. It means, although you might have to have lower efficiency solar panels, they are a fraction of the cost. Studying microbes at vents offers a lot of insight into what microbes can do. Integrated study through the use of transcriptomics, proteomics, rate measurements, measuring the geochemical changes and understanding the mineralogy, really gives us the chance to present these observations to the colleagues who really focus on the application.

Personally, I think basic research is fundamentally important. I don’t think we should do it with an eye towards application, I think we should do it for its own sake. But, here’s the catch: As soon as we’ve completed the work we can ask ourselves “how does this apply to what we need to do (as a society)”? That leads to different observations than going after something with the application in mind, because it tends to bias your perspective. I really think basic and applied research fundamentally go hand in hand in that regard.

FLG: Definitely so. Exploring these environments offers up a host of technical challenges as well, it requires a huge amount of innovation. What are the main obstacles and the main breakthroughs that are allowing us to explore these deep sea habitats?

Peter Girguis: Deep sea exploration is not for the faint of heart. There are many ways in which studying Mars is easier than the deep sea. Our atmosphere is largely transparent to radio waves and to all sorts of electromagnetic frequencies. That is why we have GPS, Bluetooth, cellular phones and radios. Many of these radio waves and other electromagnetic frequencies can leave our atmosphere and make it all the way to Mars. In fact, that’s why we could watch real-time video of a landing on the surface of Mars.

We can’t do that in the deep sea.

Traditionally, the way we communicate through water is with acoustics. That means we use modems, just like I used when growing up as a kid, and they are just as slow. What you’re really doing is kind of shouting through the ocean. You have something that is yelling that horrible sound that modems make and then there’s something that hears it, that is how we move data, at very low speeds.

Recently, engineers have been designing optical modems for underwater that transmit information through light. That means you can have something that is flashing light at a camera. You can move data at pretty close to broadband speeds and we can transmit HD video. It’s getting to the point where we can do it really well, over 50 or 100, maybe even 200 metres. But I can’t shine a light from the bottom of the ocean. I can’t even shine a light from one kilometre where the deep sea starts. So, it’s really hard to use wireless remote sensing to study the deep sea.

That being said, we’re really pushing on autonomous vehicles that can be our eyes and ears in the deep ocean. Many of us, my lab included, build a lot of sensors and samplers and are leaning on advancements in the commercial sensor space. They sell all sorts of gizmos that you can hook up to a mobile phone or with Arduinos or Raspberry Pi’s, those small low power computers, these inexpensive open design systems. We are using those to be able to put sensors into the ocean. It’s not just the highest tech such as autonomous vehicles that can sail down there. It’s also those inexpensive, simpler tools that give us a chance to make measurements without having to be there ourselves all the time.

FLG: From the seas to the stars, you’ve already touched upon Mars and the overlap there, but you’ve collaborated with NASA! A bit of a sci-fi question – is your work with them about extreme environments and the technological side, or are we preparing to do genomics with astrobiology?

Peter Girguis: There are a lot of scientists out there who are really interested in looking for life on other bodies in our solar system. I’m one of them. I’m interested in thinking about microbes. We know microbes can survive many of the conditions in space and we know that our solar system has periods when bombardment with meteorites is much higher. You can imagine if life has evolved on Earth, it could be ejected and find its way to Mars. There’s a statistical, probabilistic framework to that, but when I look at Mars, and I look at the ocean worlds, they’re very compelling areas to look for life.

Let me tell you briefly about these ocean worlds, the moons of Jupiter and Saturn. There are about a half dozen that we think have liquid water covered with an ice shell. They may or may not have hydrothermal-like activity. But the presence of liquid water means that it is in the habitable zone. We don’t know how acidic or basic it is, and we don’t know all the chemicals. NASA builds extraordinary tools for research in space, but NASA’s mortal enemy is water. Water is the one thing they do not want near their instruments at all. They build beautiful small mass spectrometers and other optical spectrometers and all these amazing tools, and they go way out of their way to make sure there’s no water vapour.

At a conference a few years ago, I presented on our own underwater mass spec and it blew their minds. I was thinking quite the opposite about how they could make mass spec the size of a thimble. So, we realised that there was an opportunity to collaborate on these missions of life detection. Ocean scientists have tools that NASA could benefit from, and the converse is true. If we are going to understand ocean worlds in our solar system, using the tools that we use to study our own ocean world makes sense. But equally importantly, is that humankind’s first life detection missions were actually in the deep sea in the late 19th century. Scientists have already been through the proverbial wringer in thinking about is life there or not there.

One of the most prominent scientists of the 19th century proposed that the deep sea had no life, the Azoic theory. It was challenged, initially by non-scientists. A very powerful scientist who carried a lot of weight in the field made this assertion and so a lot of people respectably thought he must be right. It took folks outside the field, including the retired medical doctor who was an amateur biologist, to say, wait a minute, that doesn’t make sense. That launched more and more explorations that culminated in the HMS challenger, that sailed from 1872 to 1876 on what was really ocean scientists first life detection mission, they set out to look for life in the deep sea. There is this real natural opportunity for these two communities to benefit from working with one another.

FLG: Absolutely, and to follow on in the spirit of collaboration, another passion close to your heart is increasing the accessibility of science. Can you tell us a bit about the work you’re doing in this area?

Peter Girguis: I really feel very fortunate to be where I am. I’m a child of immigrants from Egypt, who settled in California in 1969, with $150. I grew up in Los Angeles, in this aerospace town, in the height of the Cold War, where I saw what humanity was capable of. Women and men, people from different walks of life, were capable of extraordinarily things like landing humans on the moon or building a space station or a space shuttle. Now, we did it in a large part because of the cold war, but you know it brought us together – as horrible as it was. But it sort of baked in me a sense of hope that when we want to do something, we can do quite a lot by leveraging our differences. I don’t want all of us to look the same or sound the same or have the same skin colour or background.

This is true in science as well, ocean science or any science benefits from a diversity of perspectives. I don’t just mean, scholars trained at Oxford versus Cambridge, or Harvard versus Yale. That’s nonsense. What I mean is that a scientist from Tonga, or Fiji, or Bangladesh, has a different cultural framework and a different intellectual framework than I do, by definition, and they are equally valid. If we really want to better understand this ocean that runs our planet, we have got to find a better way to promote cross scientific exchange.

We do a lot of work in my lab on building tools that are affordable, on providing opportunities to scientists to sail with us on our expeditions and to try to overcome many of the structural impediments that keep us from working together. For example, there are requirements on my science funding from the United States that prohibit me from paying the salary of an Indian scientist who’s a collaborator, I can’t do that. Even though their salary is a fraction of what a US scientist might be, or even a graduate student. So, there are these structural issues that I am working on overcoming by working with the United Nations. There is currently an international treaty being developed that I hope will promote access and will benefit sharing from high seas research. Then building tools that enable people to do deep sea research in their own waters and promote crosstalk with scientists around the world.

FLG: That’s fascinating, and thank you so much for being a spearhead in that as well. As we look to the future, what are you looking forward to, as we continue to dive deep?

Peter Girguis: I am a realistic optimist, or an optimistic realist. I think that humanity has a lot of work to do, and I am not so naive as to think that we are suddenly going to become a people that can live in perfect harmony with the world. Humankind is always going to have an impact on the world, any living organism is going to have an impact on the world. But I want us to start thinking about our impact through that lens of sustainability.

I’m really hopeful in seeing early career scientists have a very different outlook than many of us did. I see a commitment to conservation and sustainability that I never saw, I never felt at their age… I had no idea. If we can get to the point where we treat Earth the way we treat a retirement account, I’ll be happy.

Let me explain what I mean. When you save for retirement, for those of us who are fortunate enough to save for retirement, your banker or planner might say you want to save enough so that you can live off the interest. So too with Earth. If we view our planet as our “principal”, and we know that our planet can only support so much productivity and create so much food, if we can figure out how to live off that interest without chipping away at the principal, I will be a very happy human. I have a lot of hope, because the scientists of tomorrow are really leaning that way, so fingers crossed for us all.

FLG: Fingers crossed, indeed. I’m going to finish up with a mean question. What is your favourite deep sea critter?

Peter Girguis: Oh, no, no, no! All right. I’m actually going to go back to my old tried and true tubeworm friends. The reason is, Riftia has many so called cousins – there’s Ridgeia, Lamellibrachia and Escarpia. These worms live in some extraordinarily diverse environments. Some live in vents, and they live fast, and they die young – they only live for a few years. The cousins of Riftia, these worms called Lamellibrachia live at methane seeps, and we think that they live to be several hundred years old. I love the idea that these two worms that are closely related, their symbiotes are almost identical, have such radically different lifestyles. I think that’s really cool because it reminds us that genomics, transcriptomics and proteomics are powerful lenses to understand organisms, but they don’t tell us the whole story. From that point of view, these worms are really closely related, but fundamentally lead totally different lifestyles. That’s pretty cool.

FLG: That’s very cool. So, thank you so much for joining me today, Pete. I have learned so much, from bioluminescence to several hundred-year-old worms and space as well. I look forward to eventually seeing the answer to that circadian rhythm question and I can’t wait to see where we will go in the future with this. So, thank you so much for joining us and taking us down the rabbit hole.

Peter Girguis: Thank you Poppy for the questions and for the invitation to join you. You have a great day.

FLG: And you, thank you so much.

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