Life beneath the seafloor: An interview with Mandy Joye

We speak with Dr Mandy Joye about her research on the deep biosphere, and the fascinating life that exists below the seafloor.


Listen to the full interview on The Deep-Sea Podcast


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dr mandy joye

American oceanographer and professor at the University of Georgia

today we have Mandy Joye. her research focuses broadly on the relationship between biochemical cycles and microbial ecology. welcome to the deep sea podcast Mandy!

Thanks Alan, happy to be here.

so let's start with a definition… what is the Deep biosphere? where is it and what size is it?

So, the deep biosphere is an incredibly vast ecosystem. It's easily one of the largest, if not the largest, on Earth. It’s starting at seafloor going down to the depths where microbes no longer exist. And that depth varies as a function of temperature and pressure and other environmental factors. But it's a incredibly important habitat for microbes on Earth and they carry out a lot of important processes that contribute to the regulation of geochemical cycles globally.

so this is everything underneath the seafloor… and this particular living space is home to things like bacteria and archaea which are enduring very extreme conditions. so, talk us through things like oxygen, temperature and pressure, and how that changes once you get below the sea floor.

Image Courtesy of Georgia Wells

Sure! So if you're in a thousand meter water column, that's 100 bars of pressure. And as you go down into the sediment column, the pressure just increases more and more and more. But then, instead of being in just an aqueous fluid, you've got sediments and pore fluid. So the sediments are getting compressed, and it actually compresses the pore fluid, which minimises the amount of microbial habitat available. The pressure itself stresses the organisms that are there, in addition to to the inherent stresses of pressure.

There are also geothermal gradients that occur in sediments, so the sediments are warming as you go down. So, temperature from the top of the ocean surface to the sea floor decreases as you go from top to bottom. But, as you go from the sea floor deeper beneath the sea floor, the temperature increases. And that geothermal gradient can be pretty shallow, or it can be pretty steep. In some places like the Gulf of California or anywhere where there's active tectonics, you can actually have hundreds of degrees Centigrade difference within a few hundred meters of the sea floor.

So temperature is a stressor, pressure is a stressor. Oxygen is rapidly consumed in sediments, so they become quickly anaerobic and inner metabolisms kick in because there's no oxygen. You've got all kinds of different ecological niches that open up as you move through this space. We breathe oxygen, right? Microbes can breathe sulfate, they can breathe iron, they can breathe nitrate. They have a number of different electron acceptors, compared to us and our our measly little one (that is oxygen).

yeah, it makes the mariana trench look easy!

I read somewhere that the inhabitants of the deep biosphere are sometimes referred to as ‘intra-terrestrials’. so please tell me that's a legitimate term and not just one made up by journalists, because it's brilliant!

No, it is actually a term that's used to describe these organisms because they are essentially living within the rocks, the sediments beneath the seafloor surface.

what does a day in the life of a deep biosphere bacteria or ‘intrA-terrestrial’ look like? OR would that be better rephrased as: what's A WEEK in the life or a month in the life or a year in a life or a decade in the Life…? what are the time scales HERE?

The time scales vary a lot because there are places in the deep subsurface where the geochemical gradients drives more rapid metabolism, so turnover times might be months to years. In other places the turnover times are as long as… as millennia. There are some places that are organic poor and there, turnover times can be thousands and thousands of years. So it's kind of hard to wrap your head around that fact. When you think about bacteria, you think about organisms that can divide every couple hours, right like E.coli? But these organisms are growing super slowly and dividing once every few hundred or a thousand years. So, they're adapted to this life in the slow lane. It requires a very different approach when you're trying to measure rates of metabolism. When we work in shallow sediments, we measure rates over a 24-hour period. But in the deep subsurface, we might have to incubate samples for a month to get an itsy-bitsy teeny-weeny signal that we can measure. It's hard to get your head around, isn't it?

it really is yeah!

So, they’re adapted to this life in the slow lane.
— Mandy Joye

when someone first took a sample from beneath the sea floor and found this bacteria, was that a Eureka moment? or was there a long period of chin-scratching going: ‘is this thing viable? what is it?’

Yeah! I mean, right now we have the International Ocean Discovery program. The original program was the Deep-sea Drilling Project, it changes every 10 years. But you know, it’s the US and the Brits and the Japanese and the Chinese and the Germans and the French. It's an international effort to drill in the deep subsurface because it is an incredible undertaking. These cruises are two months long, these deep sea drilling cruises, and you work around the clock like you you on any cruise. But it wasn't until the Peru margin Cruise (in 2004) where microbiology became a big part of the protocol.

Typically, deep sea drilling was aimed at paleo-climate research and

and others had this idea (that I think is probably it's fair to say, a lot of people thought they were crazy) that this deep subsurface had to be a really important microbial habitat. ‘What regulates it and what kinds of processes go on and what are the organisms that live there? Are they the same thing that we see in marine sediments? Are they just buried and boring? What does it look like?’

They developed this microbiology program and it was an astonishingly productive cruise. There have been many many other legs now that have promoted microbiology efforts, and now it's a standard part of these deep ocean drilling expeditions to have a microbiologist on board. Not just looking at community composition but measuring activity and looking at how these organisms process geochemicals. It's tricky because it's hard enough working in the shallow sediments of the deep sea because you're still working at high pressure, if you're in two or three thousand meters of water or at the bottom of the Mariana Trench. You want to try and replicate the conditions that these organisms experience in their natural environment. Well, when you're dealing with the deep subsurface, you've got temperature, you've got pressure, you've got chemical gradients, you've got all these things that you have to consider to really try and assess what's regulating activity. So it becomes quite complicated, but its just incredibly fascinating because sometimes there are things that are happening that you just didn't expect.

Chimneys covered in white, yellow and orange microbial mats (Beggiatoa) - Image courtesy of Mandy Joye and Schmidt Ocean Institute

we often get asked: ‘what relevance does this have? are these things actually providing a measurable ecosystem service?’ and we're almost always like ‘yes!’ because it's recycling particulate organic carbon coming down, and so on and so on.

when you get right below the sea floor, what is what is their ecosystem function?

So, everything is connected. It's just connected on different time scales. And we are biased in the time scale of an expedition or a human existence. We live in a world where time scales of days to weeks to months to years, dominate our thinking. These organisms live in an entirely different world. They live in a world where things occur slowly, but very purposefully. We have to consider that when we say okay ‘is this important or not?’ Everything is important. It's just important on a different time scale.

In places like the Gulf of California or the Peru margin or the middle of the Atlantic or the middle of the Pacific, processes are happening that recycle materials that were delivered to the sea floor. That recycling may take 10,000 years, or it may take 200 years. It depends on the conditions at that particular location.

Discharging fluids from a large flange on a hydrothermal edifice - Image courtesy of Mandy Joye and Schmidt Ocean Institute

how far under the sea floor has bacteria now been found? or microbes?

Two kilometers sub-seafloor… isn't that crazy?!

yeah! is that a one-off? a particular special Regional place or would you expect that to be anywhere?

That's not the exception, it's the rule. There's also a terrestrial oil drilling program and there have been a lot of studies in deep gold mines, four kilometers or more. And there are ecosystems down there that that are fuelled by the energy derived from the radiolysis of water.

I love to just sit around spitballing what crazy processes could exist under these conditions. It's like thinking about life on other planets or on the moons of Saturn or Jupiter. What kinds of metabolisms could exist there? That's a really interesting mental exercise because when you think about the radiolysis of water, that's like: who would have thought of that 10 years ago as a mechanism that could fuel microbial ecosystems? But now we know that this is a really common modality of microbial existence. I think that once you get outside of the box of your ordinary thinking, that's when you can really come up with some potentially interesting, if not crazy ideas to pursue.

Just like the deep sea is largely unexplored, if you look at a map of where we've drilled deep holes and where we've done detailed microbiological work, it's just a handful of sites. We drilled a lot of holes for paleo-climate research but we haven't drilled a lot of holes for microbiology. Just like the deep sea, the deep biosphere is an incredible frontier that has a lot to teach us about not just life on our planet, but life on other planets.

The deep biosphere is an incredible frontier that has a lot to teach us about not just life on our planet, but life on other planets.
— Mandy Joye


I was reading up on this a while back and it was one of the earlier papers having the first evidence that there are things living pretty far underneath the sea floor and there were sentences along the lines of ‘I think we've just doubled the living space of planet Earth’…

Right?! And it's really kind of astonishing… I teach a graduate level microbiology class and we spend a couple of weeks on the biosphere because it's a topic near and dear to my heart. During these lectures, I look out at the students and half the time their jaws are just agape because they're just astonished. They can't believe that this is part of Earth's habitable space and that it was really only discovered and probed in any kind of detail in the past couple of decades. And in those two decades we've had this genomics revolution, right? So in the beginning we were doing ‘most probable number counts’ and and stuff like that. And now, we've got the sophisticated genomic tools that we can interrogate these communities. We don't have to to isolate them and grow them in the lab, we can reconstruct their genomes on our computers. We can extract the DNA sequence for the whole community and reconstruct their genomes and look at all the potential metabolisms that exist in the community from the comfort of your desk. You don't have to go through the torture of trying to grow these organisms in the lab, because they are really tough to grow. I mean, when you're talking about an organism that has a doubling time of 500 years, I mean good lord!

what's the phylogeny of these strains? do they form a sort of unique group within the Deep biosphere or are they related to Oceanic ones or terrestrial ones?

Yes, yes and yes! So there are some organisms that are unique to the biosphere or certainly more common in the deep biosphere. There is some overlap with shallow sediments and deep subsurface sediments but there's a lot of variability. It's not like the biogeography of a fish population, there's a lot more isolation in the deep subsurface because of the time scales. I mean it's really tectonic time scales that these systems are turning over, right? It's plate tectonics that is driving it, so it doesn't really align with biogeographical patterns.

I would say that methane plays a much bigger role in a lot of these habitats because methanogens are tough. Archaea are tough in general, but methanogens are really tough. And I mean that literally because their membranes are tough as nails and they can withstand high temperatures and high pressures and all kinds of other things. I'm quite certain too, just based on the genomic data, that there are organisms that exist down there that just defy the imagination. If you look at some of the sequencing runs and the genomic symbol genomes of these organisms, they're very very different from other known organisms. And I think it's fair to say that the more sequencing we do in the deep biosphere, the more branches that we're going to be adding to the microbial tree of life.

Field of small chimneys discharging hydrothermal fluid - Image courtesy of Mandy Joye and Schmidt Ocean Institute

what about multicellular life - animals themselves? there have been some pretty surprisingly deep specimens found, are these something you would expect to find more of as a greater volume of material is brought up? or are these just rare deep-diving or deep-burrowing, deep-surviving organisms?

I think there's probably more down there than we realise… it's a absolutely a sampling issue. The way that these deep cores are drilled, any kind of animal that wasn't just perfectly aligned with the drill bit is going to just get annihilated. So we would never be able to properly sample them. The Germans have have these x-ray systems (like CAT scans) on their boats and you can look at the deep burrowing fauna. They bring these whiteboard cores up and then they just run them through the machine and be like: ‘look at that, there's some deep burrowing worms in there!’ So I think it's unfortunate that in the US Fleet, we don't have any cool toys like that. We have some cool toys… but we don't have that kind of capability. I think as that kind of capability becomes more available, maybe through philanthropy, then we can get more data like that because there's almost certainly critters that that live a lot deeper than we think they do. It's just really tough to to sample them without destroying them using the tools and techniques that we have in hand right now.

so one last question: where's This research going?

So I feel we're at a bit of a crossroads right now. Just a week or two ago, the US National Science Foundation announced that they are not going to replace the JOIDES Resolution (that's the drilling ship in the in the U.S Fleet) that's really gonna impede progress if we don't have a replacement for the J/R. I think there's still discussions underway, but right now there's no commitment for making it happen. And it's a huge vibrant community in the U.S and abroad and we need another ship because we've got a lot of work to do. It's really important and it's not just paleo climate, when you think about these organisms living under these extreme conditions, I mean the first place my mind goes to is natural products. These organisms are incredible resources for antibiotics, antivirals, potentially anti-fungals… all kinds of interesting natural products treatments for diseases. I mean, there's just there's got to be effort put towards looking at these communities. We can use this data to advance humanity in ways that weren't really imaginable even five years ago. You mentioned life away from Earth - the deep biosphere is is an obvious analog for looking at weird metabolisms and organisms that we might find on another planets. I really wish that NASA would get into this game and pick up the tab to fund some of this sort of work. I feel like we are at the cusp of making some really big discoveries because we're just getting to the point where we drilled enough sites where microbial studies have been carried out that we can start to see patterns and we can start to see trends. We can start saying ‘okay this is one of the key drivers of these communities and that really is that variable that's not so important’.

yeah if only there were some really Mega Rich billionaires with an interest in space kicking around… it seems like there's so much money going into space but not so much in terms of understanding extreme environments and how that links together

I was talking to Don Walsh about this a couple of weeks ago. And he said to me, ‘The problem with lack of funding for deep sea research, it's public relations. We just aren’t good marketers. We don't market what we do very well.’ And he's absolutely right! It's messaging and marketing and that's one of the great things about this podcast, because it gets a message out to way beyond the deep sea science community. And that's the kind of messaging that we have to work on. We don't tend to self-promote very well. I think we could be doing ourselves a big service if the deep sea science community would become more adept at science communication and learn a little bit of these skill sets that are involved than PR and marketing. I'm not talking about self-promotion, I'm talking about promoting the deep sea and the relevance of the deep biosphere.

it’s the language we use. I think the way we communicate deep sea science is really truly awful. the wording is all wrong, it's always over-sensationalised, but kind of in an empty way. you're right, it's the marketing. I think we need to take an almost corporate take on it rather than just a bunch of people who who really like it and think everyone else should really like it too.

Absolutely.

great! well, let's dwell upon the fact that biosphere is absolutely, totally, truly and utterly fascinating! it has been an absolute Joy speaking with you today mandy, and thanks very much for your time!

Thanks Alan it was great to be here. I really enjoyed it!


If you want to check out the full interview with mandy, listen to the full episode on The Deep-Sea Podcast.


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