SciCafe: Microbial Worlds of the Deep Sea with Jeffrey Marlow

JEFFREY MARLOWE (GEOBIOLOGIST, HARVARD UNIVERSITY): Thank you so much. It's a pleasure to be here and to have a chance to share some of my work. I work on the tiniest organisms on our planet. The microorganisms that are often about one one-millionth of a meter across. You can hardly see them unless you have a powerful microscope, but they are the hidden operating system of our planet. They are the ones that make things work, make everything habitable for the rest of us here on the surface. Most of my work happens in the deep sea, but before we get there I'm going to talk a little bit about a different expedition I got to go on last year. 

This was to a lava lake in Vanuatu. Vanuatu is an island chain in the South Pacific near Fiji. We were trying to answer some of these key questions about what these tiny microorganisms are doing, and what the limit of life really is around a volcano. We found ourselves kind of flying through these different volcanic island chains, across these beautiful fringe reefs of these islands, and ultimately arriving here on Ambrym Island. It's this triangular shape. There's this kind of bimodal distribution–you can see on the outside it's this beautiful lush rainforest, to the inner core are the scars of all the volcanism. These are two extremely active craters that are constantly erupting and spewing toxic gases into the atmosphere. And you can see the different kind of tendrils of lava flows from years and decades past that are fingering out from these central craters. 

We ultimately got to the top crater, and this is the summit of the island. And as you look out to sea, you see this gorgeous landscape. The different craters and different amount of vegetation are telling us how old some of these landscapes are. So this first one that we see in the center, this beautiful crater, is it maybe 2,000 years old and it's covered by this carpet of grass and orchids. But farther out, you can see in the back left there is the more lush rainforest that's about two million years old.

So we're standing on the really, really new surfaces–it's barren as far as we can tell. And progressing outward with time, we see that life gains a foothold and ultimately completely takes over. This is the view out to sea. When we shift and look toward the crater we see this. There's this constantly churning cauldron of gas. We're also again at the top of this island, so the clouds are kind of flowing in and mixing with the volcanically produce gases. And as we get right up to the surface, to the edge of the crater, we peer in and see this. This is the world's most active lava lake. There are only seven of them on our planet, and it's still a mystery to volcanologists of how the energy balance is sustained. To keep erupting, but to not release enough energy to kind of go dark. This has been going on for the last 20 years at least, this constantly churning flow of lava. And it's producing this amazing chemical cocktail. Coming out of the lava lakes of Vanuatu there's about 15% of the world's production of sulfur dioxide, and hydrofluoric acid, hydrochloric acid, hydrobromic acid, and 30% of the world's heavy metals like silver, and tin, and selenium. And the idea that life could potentially find a way to survive despite this onslaught of chemicals is very exciting and that's what we were there to find out. Our main question was if life can survive here. The next question was where it can gain a foothold and what it looks like as these samples progressed in age.

To do this we needed to get down to the bottom of this crater. This is about four hundred meters straight down this vertical cliff, and along the way we could collect samples across a range of different ages. When we got down to the bottom, this is what we were greeted with. The lava is erupting right in front of us, sometimes sending newly erupting material over our heads. We didn't want to be there very long, but this was a very rare sampling opportunity so it was very exciting. And we do know that life can find a way pretty much anywhere on planet Earth, but inside and actively erupting volcano–that's too much. The moment that these rocks cool to the point of about 60 degrees Celsius, once they stop glowing red, they become a habitable environment. Every surface on Earth is permeated by microbes. Every breath that we're taking, you're consuming about a thousand or ten thousand microbes. So they're everywhere, and we wanted to know when they could kind of gain a foothold and begin to permeate the surfaces of our planet. So we're still working to answer a lot of those questions.

But what we have found is that at a fumarole–a gas vent on the outside of this crater–it is chock-full with microorganisms. On the left here, you're seeing a scanning electron microscope image of the top layer of this sediment. We've embedded these grains in resin, sliced it really carefully, and added molecular stains that allow us to see all of the organisms and all of the ones that are metabolically active. If we zoom into this we can see these gas vesicles–so these bubbles we're seeing–that's what happens as the lava’s erupting, it's encapsulating this gas. Ultimately it cools, the gas goes away, and we retain these really juicy pockets for microbes to colonize. And if we zoom in on that tiny bit in the middle, we see what are very likely individual microbial cells inhabiting this really toxic environment on the outside of this fumarole. This was exciting. The next question, of course, is who they are and what they might be doing metabolically. We extracted all of their DNA and we sequenced their rRNA gene, this is kind of a fingerprint gene for all kinds of microbes. And we sort of plotted out what we might be seeing.

The really interesting part of this plot is the purple segment here–that's about 13% of the thousands of cells that we sequenced did not really match anything that's previously been seen. So this is kind of the microbial dark matter of the fumarole that we need to understand exactly what it's doing to potentially find new forms of life around this volcano. So that's great. But why should we care beyond the mere curiosity of this extremophile-like environment. So think about that.

I want to back up and talk a bit about biodiversity. This picture on the left is probably what a lot of people think about when we talk about biodiversity. It's a lush rainforest, it's from Vanuatu, and we're seeing, you know, maybe hundreds of different species of plants in this view. On the right we're seeing a view of three individual sand grains, and each of those green dots is an individual microbial cell. So now we're seeing thousands, or tens of thousands, of individual species around just three sand grains. So when we think about biodiversity, it depends what scale we're talking about, but also the type of organism we're thinking of. The UN has defined biodiversity as the variability among living organisms from all sources. This variability aspect is what's–I think–most important. It's not really that important, necessarily, that we name different species in different ways, but it's what they're capable of in terms of influencing our entire planet and potentially producing useful bio products. It's that variability, that functional diversity, that we're really interested in.

So let's dig into this a little bit more. This is the entirety of the math in today's presentation. We think about microbes–the estimate at the moment is that there are a trillion species of microbes. And each of them maybe has four thousand different protein-coding genes. Segments of DNA that make RNA, and make proteins. The proteins are what actually do biochemistry, so we can think about that in terms of functional units of biochemistry. On the other hand, plants and animals–the biodiversity we all appreciate and have come to know and love–there may be eighty five million species. These are often bigger organisms, so there are more protein-coding genes. But when we combine these numbers and think about the overall amount of functional diversity, the different types of proteins that could be available in these plants and animals, it can maybe be represented by this square here in green. Whereas in the microbial realm, it would be this entire slide of biodiversity.

So there's really orders of magnitude of more functional diversity in the microbial realm. And we're really just scratching the surface of what that really means. One way of thinking about life is through the movement of electrons. This is how any living thing gets energy–by transitioning electrons from one molecule to another, in the way that water going down a waterfall might produce enough energy to move a wheel. And we kind of reap the energetic windfall in each of those steps. So it's been said that, “life is nothing but an electron looking for a place to rest.” Animals, every single animal–from giraffes to penguins–are doing the same thing. We're consuming organic carbon­–like all the food we we've eaten today, and we're breathing oxygen–this is great, but it's kind of boring. It's the only thing we get to do with that metabolism. But fortunately, microbes are able to do so many other things. They can eat and breathe all kinds of chemicals. This is a very partial list–they can eat methane, ethane, toxic things to us like sulfide. And they can breathe metals, or nitrogen, or sulfate. And one of the best places to look for this type of functional diversity in terms of its metabolism, is the ocean.

That's where I've done most of my work. The ocean, of course, is hidden to us. And for the most part, we've only seen .001% of the seafloor. So there's a lot more out there, but we're already getting a sense that there are all kinds of really interesting metabolisms possible. This was from a research cruise we most recently went on in October of last year. We left from San Francisco aboard the Schmidt Ocean Institute's Falkor research vessel. And as we headed out, we kind of prepared our instruments and the way that we'd be getting our samples down at some of these deep-sea methane seeps off the California coast. We work with a remotely operated vehicle, or an ROV, shown here. It's named Sebastian, which I think is still the most clever thing ever. And it descends hundreds or thousands of meters down into the sea. It's connected by this cable, which transmits data back up to the ship, and receives commands to kind of drive around and pick up different samples. On the ship itself, we go to a control room which is just plastered with screens conveying the high-definition video from different views on the robot as well as different sensor data and navigational detection. And in the front row here we have the pilots, who are probably the world's best video game players. They're kind of controlling all these really intricate sensors and manipulators to collect really fragile microbial samples. The scientists are in the back, which is smart, get us away from the controls where we can ooh and ahh in peace, and request some of these samples that we're seeing on the screens.

And every dive shows something new. And on one of these dives we found this cliff of basaltic rock that is just covered with deep-sea corals. These could be thousands of years old–deep-sea corals might be among the oldest animals on earth, and they're found here along this cliff just kind of filter feeding on some of the nutrients that's swept by. But my favorite site is this spot called Point Dume. This is a methane seep, where a lot of methane rich fluid is coming out of the seafloor. And it’s fueling the microbial communities that make these really weird orange and white carpets and form these mounds of carbonate rock. These types of rock had never been seen before, and we've since found that the methane-consuming abilities of these microbes is maybe faster than anything ever detected before. But what's most amazing is that we were eight miles off the coast of Malibu. At night we could go up to the deck of the ship and see the glow of Los Angeles–the country's second biggest city–in the distance, and yet just eight hundred meters below the surface is this amazing wonderland that has never been seen before.

And fueling this methane seep are these symbiotic microorganisms. So I've shown them here in different stains that attach the DNA of these different organisms–so the archaea is shown in red, sulfate-reducing bacteria in green. The methane oxidizers are consuming methane and making an electron-rich intermediary that they transfer to the sulfate-reducing bacteria. We know that life is all about moving electrons around so this trading process is really favored and this entire metabolism would only be possible with this symbiotic relationship. It's operating near the edge of energetic possibility, and yet it is consuming about 90 % of the methane that's coming out of the sea floor. Methane is a really strong greenhouse gas, so if this weren't around to consume most of it, global warming would be in a much more precarious situation than it already is. So we really have these microbes to think for a lot of that. The end result is bicarbonate, which precipitates with calcium in the seawater and makes rock. So these microbes are building these mounds of limestone and kind of changing the whole topography of the seafloor in the process.

The seafloor is the best place to find some of these exotic microorganisms because of the gradients of electrons that happen down on this surface. So I like to think of the earth as a big battery, where in the subsurface–the mantle and the lower portions of the crust–we have fluids that have a lot of electrons; and here on the surface world–in the ocean or in the atmosphere–it's areas with very few electrons. So at that boundary zone, microbes are able to kind of really make a living by making that trade of electrons from the rich subsurface to the electron-poor surface world.

There are kind of three flavors of these chemosynthetic hot spots on the seafloor. One are the black smoker hydrothermal vents–these are probably the ones you've seen most about. They're really hot, they’re 200 to 300 degrees Celsius. They're rich in metals, the second that this metal-rich fluid gets into the water it precipitates as oxides–that's the black smoke that we see–and it fuels this rich oasis of chemosynthetic life like these big tube worms. Methane and other hydrocarbons seeps are my favorite, that's what I spent most of time studying. And again, these are spots where a lot of methane, ethane, and propane even is coming out of the seafloor, potentially into the atmosphere. And finally, there are these lost-city type hydrothermal systems. They're alkaline in pH, there have only been two or three of them found so far. They aren't really in the types of geological environments you'd expect to see hydrothermal activity, but they're amazing and they are fueled by this abiotic chemistry that is actually pretty suggestive of where life might have originated and where we might find it beyond Earth.

So again, these sites are usually out of sight out of mind for us, but the microbial communities that sustain them drive a lot of important ecosystem services for us here on the surface. They move elements through them, so key elements that we all need to survive: nitrogen, sulfur, phosphorus, oxygen, they often go through this microbial pump. They produce the base of the pyramid that then allows other larger organisms to eat them, ultimately building up commercially relevant fisheries that we all depends on. They comprise enormous genetic resources–we already saw that their genetic diversity is so much higher than the plants and animals we’re mostly familiar with on earth. And this is where the drugs of the future will almost certainly come from. The polymerases that allow DNA sequencing to happen–the most advanced one–have been found from deep sea hydrothermal vents. A lot of this gas coming from the sea floor is our greenhouse gases, methane being the most prominent. The fact that these microbes are able to consume that is really important. And, again, especially at this lost city environment, it might be where life first gained a foothold. The kind of chemical and geological proto-cells that form naturally could help make for those gradients that allow protons and electrons to flow across and through them and allowed the initial signs of life to maybe gain a foothold.

So this is really exciting. These are a few of the types of spots that we see, but we've again only seen a tiny, tiny fraction of the seafloor and every day there are amazing new environments being found. This is from a research cruise last November. Right after we got off the ship in Southern California, other researchers got on, went to the Gulf of California, and found this insane place where there's all these really hot fluids coming out and precipitating these really fragile carbonate lenses, and then this reflective fluid forms because of the different densities inside. If you look at just the right angle there's this cell FIDIC crust that forms–it's this amazing combination of both hydrothermal activity and hydrocarbon activity, so kind of blending a couple of those types of chemosynthetic environments I was talking about. So this might be the fourth type of this, and it's really only been found in the last several months.

The concerning thing is that a few of hours after this video was taken, they were poking around other parts of the Guaymas Basin and found all kinds of trash. There were deflated mylar balloons, there were plastic bags, there were even discarded Christmas trees. So even the places that we've never even seen before are already being affected by human activities. There was a study a few years ago where in the Mariana Trench, the deepest ocean basin we have, scientists collected small crustaceans and analyzed the composition of their shells and found PBCs–industrial pollutants–from years past. The problem, of course, is that the we've been doing this for decades and centuries and the global conveyor belt that is the atmosphere in the ocean mixes all these pollutants before we even have a chance to characterize these environments for the first time. Fortunately, there is a glimmer of hope. And that is happening at the UN. There are currently negotiations going on to conserve the biodiversity in the high seas–these are the areas of the ocean that are beyond any given country's territorial waters–that's about forty-five percent of planet Earth. And at the moment it's kind of the Wild West out there, there's no comprehensive set of laws to govern what happens out there. The open ocean and the high seas have been enshrined in international law to be kind of governed and available to the common good of all humankind, and there are really important, complicated, really boring regulations that we need to discuss that will ultimately set the framework for these really important issues. So it's things like the marine genetic resources, the transfer of technology, how we do our environmental impact assessments, the intricate language around each of these can be tough to hammer out but it's happening right now and it's really a once-in-a-lifetime opportunity to conserve these areas.

The biodiversity that already exists on the seafloor is doing things we don't often appreciate. We're still just scratching the surface of what's even there and what they might be doing, and already we're affecting these areas before we've even seen them. I think there's a new urgency among the oceanographic community to really get out and see some of these new places that we've never seen before, before it's too late to really conserve them. Thank you very much.