Biocryomorphic evolution on the Greenland Ice Sheet

Our new paper, “Metabolome induced biocryomorphic evolution promotes carbon fixation in Greenlandic cryoconite holes” came out this week. The main finding is that cryoconite holes can change their shape in three dimensions to maintain comfortable conditions for microbial life – an example of biocryomorphology in action. Here’s a summary of the main points:

  1. Cryoconite holes change their shape and size according to environmental conditions. A mechanism for this, driven by nonuniform arrangement of cryoconite granules or receipt of solar radiation, is presented.
  2. Changes in hole shape are accompanied by changes in metabolic processes in microbial communities on the hole floors
  3. Cryoconite systems tend to evolve towards wide, flat floored shapes where cryoconite granules are spread out and able to photosynthesise more. This means cryoconite holes naturally maintain conditions conducive to capturing carbon.
  4. When these equilibrium states are disturbed, the microbes become stressed, send molecular signals to each other and quickly employ metabolic survival strategies.
  5. A possible mechanism for the migration of cryoconite holes away from shade implies biocryomorphic regulation of hole floor conditions for populations of holes.
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Making cryoconite hole measurements with co-author Tris Irvine-Fynn (ph. A Edwards)

This paper indicates the potential for combining ice physical, biogeochemical and molecular (in this case metabolomic) analyses in gaining a mechanistic understanding of Earth’s ice as a ‘living landscape’. Another recent paper by Bagshaw et al (Cardiff Cold Climate) examining cryoconite responses to light stress at the other end of the planet is available here.

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GRIS 15 Diary: Part 4

Thanks to British Society for Geomorphology, Gino Watkins Memorial Fund, Gilchrist Educational Trust, Mount Everest Foundation, Andrew Croft Memorial Fund, Scottish Arctic Club and Gradconsult for supporting this field work. Thanks also to the GRIS15 field team: Ottavia Cavalli, Michael Sweet and Arwyn Edwards.

The team working at the field site, ca. 3 km from the margin of the SW Greenland Ice Sheet, captured using the DJI Phantom Vision 2 + drone.

July 13th

Despite the mosquitoes, Greenland is a beautiful place. The rocks glisten with flecks of pyrite, the lake waters are beautifully clear, the rivers are turbid with glacial flour and as the season progresses the green land is becoming freckled with blooms of cotton flowers. We have seen Arctic foxes and reindeer. The ice is spectacular, changing colour throughout each day as the melt rate waxes and wanes. Melt pools grow and shrink, cryoconite holes deepen and shallow, supraglacial streams swell and shrink and migrate across the ice surface. The colours are whites and blues to greys and greens. It is a magical, beautiful place and we are very lucky to be working here. Today’s field work went well. We are ahead of schedule on our science goals and the data is looking good. No sign of the weather changing at the moment either, so we are putting our heads together to come up with more ideas to extend the science programme and make the very most of our time here. When we arrived back at camp to find fellow glacier researchers Marek Stibal, Karen Cameron, Jakub Zarsky and Tyler Kohler (collectively @CryoEco) at camp. It was good to catch up and find out a little about their field season over at Leverett Glacier.

 

A Greenland lake in summer bloom (ph. M Sweet)
A Greenland lake in summer bloom (ph. M Sweet)
Cotton grass near the ice margin (ph. M Sweet)
Cotton grass near the ice margin (ph. M Sweet)
Midnight sun over a glacier-fed river
Midnight sun over a glacier-fed river

July 14th

Today was another productive day in relatively good weather. Another solid day’s worth of data was recorded by all members of the team. Everything ran pretty much according to plan. I had a look over the data so far and am hopeful of some good results, but it will require some deep analysis once back in the UK. I have been sleeping badly since we got here, largely due to the midnight sun and tonight was especially bad. I walked down to the river and read my book in the early hours and it felt like midday.

Cavalli, Edwards and Cook en route to the site (ph. M Sweet)
Cavalli, Edwards and Cook en route to the site (ph. M Sweet)
Observing a cryopond at the site
Observing a cryopond at the site

July 15th

My initial science objectives were met today! The weather has been extremely kind to us thus far and our productivity has been higher than expected. I plan to continue to make further measurements and expand the dataset, whilst also establishing some associated extension experiments. Today was hard going though. The katabatic winds were right back up to full strength and it was bitterly cold at the site, especially once my hands had been in a few cryoconite holes! We are all starting to feel tired after a long stretch of continuous field work, but the end of the first observation period is in sight and everyone’s primary science objectives should be in the bag in the next couple of days.

Otti at work (ph. A Edwards)
Otti at work (ph. A Edwards)

July 16th

Another hard day weather-wise. It is really the wind that makes things difficult and slows us down. It’s also hard work to stabilise the drone in the wind, and I doubt we will have much useful imagery from these very windy days. Thankfully, there have been enough calm days to ensure sufficient data capture, and more importantly, we haven’t lost or broken the drone! Again, I decanted samples into falcon tubes to process back at camp, and the mosquitoes made it very unpleasant. Still, it got done and as a team our minimum science aims have now been met. This is quite a weight off our minds, since data collected from here on in is largely bonus and if the weather or logistics turned against us from tomorrow onwards, we can still be assured of returning home with some science achievements and data to work up in the autumn.

Otti and Arwyn doing lunch
Otti and Arwyn doing lunch
Mile and I: drone selfie
Mile and I: drone selfie

July 17th

We finally took a bit of a rest day today, and gained a new recruit to our camp. Leo Nathan is an MSc student at Aberystwyth University who is working under the supervision of Prof. Alun Hubbard. Leo is flying fixed-wing UAVs over long transects to generate Digital Elevation Model data of several of the rapidly melting glaciers in this region. We visited his original camp, up near Point 660, where he has been building and launching the drones. It was all very impressive stuff, and Leo was very knowledgeable and happy to talk about the project, and made a welcome addition to the team.

Field site panorama (M Sweet)
Field site panorama (M Sweet)
The team by one of many dramatic and picturesque cryoponds (M Sweet)
The team by one of many dramatic and picturesque cryoponds (M Sweet)

July 18th

Today was a final day of measurements at the original field site and was relatively routine. Leo cooked dinner tonight and it was a damn fine spaghetti bolognese (although our resident Italian may disagree)!

Dr Edwards in a bag
Dr Edwards in a bag

July 19th

Today we pulled our equipment out ready to change field site. This meant dismantling the loggers we had set up, collecting in pieces of equipment and markers, and generally leaving the place as pristine as we found it. This took the morning and we were off the ice just after 1pm. We had some lunch and then went to another nearby glacier to scope out possible access points for obtaining some basal ice samples. On the way we encountered a family of six musk oxen, including two very small calves. Mike and I took a walk over to another nearby glacier and watched the calving ice for a while before dinner. The sun is starting to get lower in the sky at night now, and this evening was especially beautiful down at the river. I sat there and read until it was late and eventually too cold to be out of a tent.

One of the bigger musk ox (M Sweet)
One of the bigger musk ox (M Sweet)
Musk ox family (M Sweet)
Musk ox family (M Sweet)

July 20th

Today was Otti’s final day in Greenland with us. To make it a good one, we took a trip to Russell Glacier, where we watched the glacier calve. This site has changed dramatically since my last visit in 2014, having undergone some major calving and slumping. If there is some out there, I’d love to see some time lapse imagery of this piece of ice. We had some lunch and did some reconnaissance for a future research idea before walking out. Back at camp, we had a good sort out of our field kit, rearranged the tents and packed up gear that Otti would take back to the UK. We also organised the equipment that the remaining team members would need for the rest of the trip and nailed down some further research plans for the final leg of the trip. I stupidly fell asleep out in the open and woke up having been feasted upon by mosquitoes – my face looks like a sheet of bubble wrap!

The calving face of Rusell Glacier
The calving face of Rusell Glacier
The ice cave and calving face of Russell Glacier
The ice cave and calving face of Russell Glacier

July 21st

Today was not a good day. We awoke as usual and ate breakfast, then piled into the truck to drive Otti to town in time for her flight. About 12 km from Kangerlussuaq we were involved in a collision with another vehicle and had to evacuate to KISS. Thankfully nobody was hurt, but there was damage to both vehicles. A police report was filed and the rest of the day was spent trying to contact relevant insurance agencies and our university contacts.

July 22nd:

Today we necessarily stayed in KISS to try to sort out the vehicle issues. While we wait, the last of pour funds are evaporating in accommodation costs, plus food etc and we are without a vehicle to get to a field site to extend our science! We also have the additional problem that our camp is still established at the ice margin… Late in the evening two cancellations were made for tomorrow’s flight out of Kangerlussuaq, so Arwyn and I snapped them up. With Otti already home safe and sound, and Mike’s flights only two days away anyway, this was seen as the most prudent damage limitation option. An extremely kind offer of a lift out to decamp by a University of Essex research group meant we could quickly get our kit packed up in time to bail tomorrow.

July 23rd:

It is with heavy heart and light wallet that we leave Greenland today. However, we managed to achieve our primary science aims before disaster struck, and everyone is leaving injury free. So overall, although we are a few days early retreating from Greenland, we have the data we need to produce our manuscripts as planned and have loads of images and footage for outreach and analysis. We have met some great folks and seen an incredible part of the planet, and should produce some good publications as a result. However, two secondary objectives that were scheduled for the last few days were not met: depth sampling in a crevasse and bulk sampling of cryoconite. Things could have been a whole lot worse and we are now looking forward to getting stuck into analysing and writing up our findings!

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Thank you’s:

Another huge thank you to our funders  British Society for Geomorphology, Gino Watkins Memorial Fund, Gilchrist Educational Trust, Mount Everest Foundation, Andrew Croft Memorial Fund, Scottish Arctic Club and Gradconsult for supporting this field work.

I also thank Professor Alun Hubbard, Leo Nathan, Johnny Ryan and the team from the University of Essex for their company and/or collaboration.

Finally, my thanks go out to the GRIS15 team: Ottavia Cavalli, Michael Sweet and Arwyn Edwards.

NEP Video

Here is a quick video I made outlining the well-known “total dissolved inorganic carbon” (TDIC) procedure for measuring Net Ecosystem Productivity.  It is a very basic aide-memoir for undergraduate and postgraduate students showing the major steps in the TDIC procedure. There is a paper document to accompany this video available to students working in the labs at the University of Derby (available to others upon request). You may also like to read this.

This was filmed at Camp Dark Snow in summer 2014. Field work was undertaken there with the support of the Gino Watkins Memorial Fund, Andrew Croft Memorial Fund, Scottish Arctic Club, Royal Society Research grant (PRESTIGE to Arwyn Edwards) and support from the Dark Snow Project.

The LEI team at the University of Derby (esp. Matt Howcroft and Hannah Davies) supported the production of this film.

New Scientist’s “Icy Oases” Article: The full interviews!

New scientist recently published an article introducing cryoconite holes as oases for microbial life on ice surfaces. As ‘new scientists’ working on cryoconite, colleagues Arwyn Edwards (Aberystwyth University), Karen Cameron (GEUS / Dark Snow Project) and I (University of Derby) were interviewed by science writer Nick Kennedy. Of course only a few sound-bites made it into the final article, so here I present mine and Arwyn’s answers to Nick’s questions – in full – to provide further detail for intrigued readers. 

NK = Nick Kennedy, AE = Arwyn Edwards, KC = Karen Cameron, JC = Joseph Cook

video credit: J Cook, H Davies (LEI – University of Derby). With thanks to Arwyn Edwards, Tris Irvine – Fynn, Dark Snow Project, Gino Watkins Memorial Fund, Andrew Croft Memorial Fund, Scottish Arctic Club and Royal Society.

NK: What is the most fascinating creature in cryoconite holes for scientific purposes? What about just because of peculiarity/oddness? Presumably there’s several unusual adaptations that enable them to survive there.

JC: There are several species of particular interest inhabiting the cryoconite holes. Firstly I’d propose the Cyanobacteria that are apparently ubiquitous in cryoconite worldwide – not because they are unique to cryoconite (far from it!) but because of their vital role as ecosystem engineers. These microbes are filamentous, allowing them to capture and entangle mineral and organic matter to form coherent granules. They are the dominant primary producers that provide food for several trophic levels of biota and as a by-product of their activity they form stable microhabitats that enable diverse microbial communities to develop.

In terms of peculiarity, it has to be Tardigrades. These are commonly referred to as “water bears” and usually represent the highest predators in cryoconite communities (although midges and some insects have been identified on some mountain glaciers). They are incredibly hardy creatures that can remain active in deep ocean, high mountain and deep englacial environments and have even survived periods in the vacuum of space!

AE: My Biology students at Aberystwyth University love tardigrades. It’s hard not to as they have a certain anthropomorphic appeal. However, I find rotifers, which are also present in cryoconite to be the most intriguing. We know they have been asexual for an estimated 80 million years, and believe that must make radical rearrangements to their chromosomes to survive. Not even tardigrades go to the extent of rearranging their genomes to survive.

Scanning electron microscope image of a live “water bear”. Ph from "Eye of Science"
Scanning electron microscope image of a live “water bear”. Photo: Nicole Ottawa & Oliver Meckes / Eye of Science / Science Source Images

NK: Do we have a lot to learn from these highly adapted species?

AE: I would like to think so. DNA sequencing tells us there are hundreds to thousands of species of microscopic life in cryoconite, biodiversity levels comparable to soils even, and we know that that the total community’s metabolic rate (technically its rate of carbon production) equals that of some Mediterranean soils. But all of this is happening in a temperature range between 0.1°C and 1°C in the active growing season, which would be thermodynamically very unfavourable relative to, say, those Mediterranean soils. We therefore assume that the organisms in cryoconite have lots of adaptations to these extreme conditions. But, to date – we don’t know what these adaptations are.

The beautiful cryoconite at S6, Greenland ice sheet
The beautiful cryoconite at S6, Greenland ice sheet

NK: Are cryoconite holes contributing to glacial melt? Is that influenced by the organisms that live in them?

JC: This is a very interesting question, without a simple answer! The key issue is the reflectivity, or “albedo” of the cryoconite. Because cryoconite is dark (i.e. it has low albedo), it efficiently absorbs solar radiation and transfers that energy to the underlying ice, accelerating it’s melt rate. It is precisely this process that leads to cryoconite hole formation. However, when cryoconite holes form, they fill with melt water and hide the dark granules beneath a layer of reflective water, reducing their albedo-lowering effect on the ice surface. While cryoconite definitely does have an albedo lowering effect, and cryoconite holes do darken the glacier relative to clean ice, dusts and algae that remain upon the ice surface between cryoconite holes have the greatest darkening effect (see Yallop et al, 2012) and the evolution of both cryoconite granules and cryoconite holes can lead to complex patterns of melt.

The organisms that live in cryoconite granules strongly control their albedo. Inert mineral dusts are darker than clean ice but they have much lower albedo when they are encased in organic matter in cryoconite granules (see Takeuchi et al, 2001, 2002, 2010; Tedesco et al, 2013). This organic matter includes cyanobacterial biomass that entangles dusts, soot and organic matter along with biological “cements” that glue the organic and inorganic materials together into coherent granules. In addition, heterotrophic bacteria feed upon organic matter and produce dark, sticky humic substances and some microbes produce dark pigments to protect themselves from intense sunlight. All of these processes darken the granules and enhance their ability to absorb solar energy and locally accelerate glacier melt rates.

What is most fascinating (to me) is that the formation of these dark granules is ultimately a biological process, and the result is the formation of cryoconite holes that can change their shape to maintain favourable light intensities on the hole floors and therefore promote photosynthesis (see Cook et al, 2010). This allows cryoconite to support diverse and remarkably active microbial communities in an otherwise hostile environment – a great example of ecosystem engineering (see Jones et al, 1994) that arises from locally accelerated melting of ice.

AE: The answer here is a clear yes. We have known for about fifteen years that microbially-formed pigments in cryoconite darken it and that this is a significant contributor to glacial surface melt, both on valley glaciers, and thanks to more recent work, the Greenland ice sheet. Vast swathes of the Greenland ice sheet are covered in cryoconite – even visible in satellite imagery – and so we have strong evidence that the biological darkening of ice is an important feedback in melting. Unfortunately, climate models assume that all impurities on the ice surface are black carbon, and thus do not capture the effect of biology, or its consequences stemming from the impurities being alive and growing…

Greenland ice sheet melt in action: observing surface runoff in a stunning supraglacial stream (ph. Sara Penrhyn-Jones)
Greenland ice sheet melt in action: J Cook observing surface runoff in a stunning supraglacial stream (ph. Sara Penrhyn-Jones)

NK: If there’s life hiding in such tiny dust particles on an otherwise inhospitable land, could we see something similar on other planets?

JC: It is possible, and there are several research groups that look specifically at the astrobiology of other icy places in the solar system. Antarctic ice is commonly cited as a Martian analog because it is the coldest, driest place we can currently access. The cryoconite holes in Antarctica are different from elsewhere – because the temperatures are so low they are completely entombed in ice, melting small pockets of liquid water under the surface thanks to a solid-state greenhouse effect. This effectively isolates them from chemical exchanges with other environments and promotes the development of rather extreme hydrochemical conditions (see Tranter et al, 2004). These holes in particular might be good analogs for potential habitats elsewhere in the solar system.

AE: Potentially, yes. Cryoconite holes are self-stabilizing systems. Their albedo-reducing effect is strong until they melt to a depth which has the same melting rate as the ice surface. Meanwhile, the microbe-dust aggregates tend to rearrange themselves laterally to become a single layer thick. The net result is an microbially-mediated system which sits at its optimum depth for photosynthesis (not too deep to have too little sunlight, not too near the surface to be irradiated by UV), and “ensures” that as much of its surface area as possible is exposed to promote photosynthesis. As such, it presents an elegant example of how life can promote conditions to sustain itself, even in otherwise hostile environments.

NK: Could these organisms be life’s stowaways that might soon populate other areas covered in ice (do these occur on the polar caps, too)? Would they change the local flora and fauna thanks to hitching ride in these dust bits?

JC: Cryoconite holes exist on almost all ablating ice surfaces – they are a near-ubiquitous feature of melting ice. This includes ice sheets and glaciers in the Arctic, Antarctic and smaller valley glaciers at lower latitudes (e.g. Alps, Himalaya, Tien Shan, Andes). It has recently been recognised that they are not isolated habitats, but are actually part of a dynamic glacier-wide aquatic ecosystem comprising microbes and nutrients flowing through porous ice near the glacier surface (see Irvine-Fynn et al 2013; Edwards et al, 2014). The cryoconite holes can be thought of as sites of favourable conditions for photosynthesis and therefore enhanced microbial activity and biodiversity within this spatially expansive aquatic ecosystem. These habitats migrate, divide and coalesce throughout a melt season, while the microbes within them change their community structures and biogeochemistry in response to changing environmental conditions. Their role as ecological entities is therefore complex and there are certainly fluxes of cells both into cryoconite holes from other environments and also out of cryoconite holes to other environments. Given that glaciers are receding and the planet will deglaciate ever-more rapidly in a warming climate, the microbes inhabiting cryoconite holes will increasingly be delivered to newly exposed land, glacier fed streams, lakes and the oceans, with currently unknown impacts upon the ecology of those environments. Glacial sources contribute significantly to the flux of organic carbon from the land to the ocean (see Hood et al, 2009), but the role of cryoconite microbes in the storage, release and transformation of that carbon is still unknown.

Millions of cryoconite holes occupy melting ice surfaces on the Greenland Ice sheet
Millions of cryoconite holes occupy melting ice surfaces on the Greenland Ice sheet

NK: Do cryoconite holes affect carbon dioxide levels?

JC: Microbes in cryoconite holes are remarkably active, especially considering they exist in conditions of low nutrients and low temperatures. Some studies have suggested that they cycle carbon at rates comparable to Mediterranean soils (see Anesio et al, 2009). Major differences in carbon budgets exist in different geographic regions. As a general rule cryoconite holes on low gradient, slow moving, stable ice in the interior zones of large glaciers and ice sheets seem to be carbon sinks, whereas cryoconite holes on steep, fast moving, dynamic ice on valley glaciers and at the edges of ice sheets are more likely to be carbon sources (see Stibal et al, 2012). Stability seems to favour net carbon drawdown from the atmosphere. Whether these fluxes are of significance to large scale atmospheric carbon concentrations is still to be firmly established. Several estimates of cryoconite carbon fluxes have been made (see Anesio et al, 2009; Hodson et al, 2010; Cook et al, 2012) but they were based upon linear extrapolations of very limited empirical data and do not take into consideration any bio-glaciological feedbacks or changes in microbial activity over time. Given that there are billions of cryoconite holes covering the melting parts of glaciers and ice sheets worldwide, and the rates of carbon cycling within them are surprisingly high, it is possible that these features affect atmospheric carbon concentrations, but this remains uncertain.

AE: Cryoconite holes are important as ice-cold hot-spots of carbon sequestration on glacier surfaces. We have no clear idea about their contributions to the global carbon cycle in quantitative terms beyond early, limited datasets which based their assumptions on linear extrapolations. What we do know though is that these are organic-carbon hot-spots in carbon limited environments: both the glaciers themselves, and downstream environments like coastal seas and glacier forefields, so the cryoconite carbon cycle can have strong regional influences. Finally, much of the organic carbon present is “dark”, as proto-soil pigments formed by microbial decomposition or microbial pigments. The impact of this dark carbon on ice melt is important (as mentioned above).

transfers of organic carbon and viable cells occur between cryoconite covered glaciers and other nearby environments including proglacial streams and newly deglaciated land.
transfers of organic carbon and viable cells occur between cryoconite covered glaciers and other nearby environments including proglacial streams and newly deglaciated land.

NK: How will this change with climatic change?

AE: We know that cryoconite microbial aggregates are an intermediate to mature stage of colonization of glacier surface, a process which starts with microbial (often algal) growth on snow and bare ice. There is the notion that the microbial feedback to ice-melt from cryoconite represents a biological pre-conditioning of a glacier to its death by the accumulation of microbial biomass which can then establish itself in nearby habitats (forefields and coastal seas, as above). We therefore expect glacial systems to be increasingly biological as they decay thanks to climatic change.

NK: Might there be a host of species in cryoconite holes that may never be classified or seen?

AE: I’m an optimist, so I would never say never. However, there is an element of truth to this, but that which is true for many if not most natural environments as far as microscopic biodiversity is concerned. It is only through the rapid developments in high-throughput DNA sequencing technology that we are aware that glaciers have any biodiversity at all. At first glance, glaciers are not the Amazon. But we know now that there are more microbes in the top metre or so of glacial ice than in rainforest soils. As glacial ice holds 70% of Earth’s surface water, they are its major freshwater ecosystems. But of the 198,000 or so glaciers on earth, we only have DNA data published from 20-30 of these sites.  Moreover, our ability to sequence the DNA of all life-forms present is technically limited. We can reliably detect the hundred or thousand most dominant, but rare organisms are easily missed.

Personally, although we have some interesting discoveries about eukaryotes, I am most puzzled about the Archaea associated with cryoconites. We often think of Archaea as the experts at surviving extreme environments, and we know that methanogenic Archaea are prevalent beneath glaciers. But it is very difficult to detect Archaea in cryoconite, and we have only a few reliable reports. Either they are generally absent, or the Archaea there are too different to be detected by our DNA sequencing experiments for some reason.

NK: In what ways are the anabiotic qualities of organisms found in cryoconite holes interesting to biotechnological science?

AE: Dormancy (=anabiosis) is an interesting phenomenon from an applied perspective. Some of the adaptations concerned with becoming dormant are relevant for protecting freeze-sensitive materials such as drugs or vaccines, for example the production of “cryoprotectant” molecules, and as far as microbes are concerned, there are common dormancy and revival mechanisms between some of the bacteria in cryoconite and medically-important pathogens which are latent in human hosts for many years, such as tuberculosis.

JC: Adaptations related to anabiosis might make cryoconite important for bioprospecting and biotechnology; however, this has not really been explored in depth. It seems reasonable to suggest that organisms that utilise anabiosis to thrive in hostile conditions of low temperature and low nutrient concentrations might have adaptations that could be exploited by biotechnologists. For example, harvesting anti-freeze proteins could potentially be useful for cryo-preservation.

Many thanks to New Scientist, Nick Kennedy, Arwyn Edwards and Karen Cameron

Water Bears on Ice: Guest blog by Jesamine Bartlett

Huge thanks to Jesamine Bartlett – a recent MSc graduate from the University of Sheffield who has been working on Tardigrade research – for providing this introduction to the weird world of water bears…

Scanning electron microscope image of a live “water bear”. Ph from "Eye of Science"
Scanning electron microscope image of a live “water bear”. Ph from “Eye of Science”

Whether or not you like microbiology, bugs, or even science, no one can deny the frankly awesome nature of the Tardigrade. Even the tabloid press are fans!  Tardigrades are small, inconspicuous invertebrates that live quietly in almost every habitat we know of. If there is water, there will be probably be active Tardigrades. Even where there isn’t water they have a remarkable ability to enter a hibernation state that allows them to survive freezing and drying out. They have been found at both poles, 20,000ft up mountains in the Himalaya to 14,000ft deep on the ocean floor (Everitt, 1981; DeSmet & Van Rompu, 1994; Ramazzotti & Maucci, 1983; Renaud-Mornant, 1982 ). They are as close as residents in your back garden and as far out as visitors to outer space! More on that later…

Known as moss piglets or water bears because of their clawed legs (called lobopods) and lumbering bear-like gait, the Tardigrade is a tiny creature that measures on average 500µm when adult. They are small enough that you can’t see them with the naked eye, but large enough that you can easily extract them from moss and view them with a good hand lens or simple microscope. Similarly to many invertebrates with a hard outer cuticle, they grow by moulting. This process is known as “ecdysis” and is the same process as spiders shedding their skin. Often Tardigrades take advantage of this discarded hard outer shell by laying vulnerable eggs inside them for protection.  Tardigrades reproduce sexually, with females either laying the eggs in the moult with the male fertilizing them afterwards, or through internal fertilization and eggs lain afterwards. Tardigrades can also reproduce via “parthenogenesis” – a hermaphroditic “female” fertilizing her own eggs internally. Tardigrades are generally omnivorous, eating plant cells, algae and also other microscopic invertebrates such as rotifers or even other Tardigrades. Having a flexible diet that relies on no single food source helps water bears to exist in such disparate places across the globe. Because of their ability to survive pretty much anywhere, Tardigrades are one of comparatively few multicellular animals to earn the status “extremophile”, a label that is usually attributed to bacteria and archaea that can happily live in extreme environments such as deep sea hydrothermal vents, or trapped deep in glacial ice with little or no oxygen. Since extremophiles live in such rare and inhospitable conditions, they can tell us about the ranges of conditions where life is possible.

Live Tardigrades extracted from Arctic cryoconite – Credit - Jesamine Bartlett
Live Tardigrades extracted from Arctic cryoconite – Credit – Jesamine Bartlett

Tardi 2

Over the last few decades, the extreme habitats at Earth’s poles have attracted increasing research attention. Complex life has now been identified on, in and beneath Arctic, Antarctic and mountain ice (Wharton et al, 1981; Kohshima 1984; Hodson et al, 2008). Recently, fish were even discovered living beneath lake ice in Antarctica (see also Brent et al 2014), illustrating the potential for previously undiscovered complex life on Earth. At the poles, Tardigrades inhabit deglaciated terrain, and the surfaces of glaciers and ice sheets. Living in and under ice is extreme in the highest degree, with low nutrients, low light, low temperatures and high pressures. But it is comparatively stable to that of the surface; Frequent and drastic environmental fluctuations including periodic freezing and thawing, glacier hydrology, meteorology and intense irradiance challenge incumbent microbes, some of which develop specific physiological adaptations that allow them to survive. In order to survive extremely low temperatures (for example on ice surfaces during winter beneath a seasonal snowpack). Tardigrades enter a state of “cryptobiosis”, slowing their metabolisms to ~0.01% of normal and losing up to 99% of their total moisture. This cold, dry hibernation state is known as their “tun” state. The cessation of metabolism to such levels would kill most animals, but Tardigrades can amazingly reverse this state, blurring the line between living and dead. In the presence of liquid water, such as a spring thaw, Tardigrades can awaken, rehydrate and reanimate themselves. While in the tun state, a Tardigrade can survive for years in adverse environments, and after 10 years most can fully reanimate and continue their life cycle as if they had only just stopped to have a nap. The record for reanimation is 120 years in tun state – although the Tardigrade in question didn’t survive very long after awakening. As a tun, Tardigrades are light, dry capsules of their former selves, capable of being transported about by wind, animals and perhaps even asteroids, which to some extent revived the Panspermia hypothesis – that life on Earth was brought here by a ‘hitchhiking’ organism (Jönsson et al, 2008; Pasini, 2014).

Scanning electron microscope image of a Tardigrade in its dehydrated “tun” form.  Ph. credit - Eye of Science
Scanning electron microscope image of a Tardigrade in its dehydrated “tun” form. Ph. credit – Eye of Science

The ability to survive in the extreme cold, even close to absolute zero in some experiments, has led to Tardigrades being studied for their viability in space. In 2007, the European Space Agency (ESA) sent live Tardigrades and unhatched eggs into the vacuum of space beyond the International Space Station, where they orbited the Earth for 12 days, fully exposed to the full spectra of solar radiation. They called the programme “Tardigrades in Space”, or TARDIS for short to the acclaim of many a Dr Who fan!  The eggs hatched unharmed and 68% of the adult Tardigrades reanimated with no apparent ill effects. In preparation for a potential launch to Mars in the coming decade through the ExoMars programme, the ESA are currently recreating Martian environments to test the Tardigrades under. So you can be assured that they will continue to be a key to exploring the possibilities of extra-terrestrial life in the future.

One of the keys to a Tardigrade’s ability to reanimate from a tun state and survive such extreme habitats seems to be their ability to turn glucose sugar into trehalose sugar (Teramoto et al 2008). Trehalose is a disaccharide cellular sugar found throughout the natural world that helps prevent molecular desiccation (the process of cell deformation and rupture from drying and/or freezing). Trehalose stores water in a “gel phase” that can form a supportive cast around cell walls and organelles, preventing them from distorting and also reduces the amount of un-bonded water available for freezing.  Converting blood sugars into trehalose is not unique to Tardigrades. Bees switch between glucose, trehalose and sucrose depending on their metabolic rates (Blatt & Roces, 2001). Trehalose does not fully explain the resilience of Tardigrades, however. It is still unclear how they withstand drastic fluctuations in solar radiation, pressure or temperature and survive to produce healthy offspring. Understanding these processes might help scientists find ways of better preserving living tissues, whether that is human eggs for fertilization, organ transplant, maybe even one day full human suspended animation!

The physiology of Tardigrades therefore make them extremely interesting invertebrates, but they are also significance players in many ecosystems, in particular the truncated food webs at the poles. And it is in cryoconite holes that Tardigrades are able to thrive on ice. These habitats provide favourable conditions for primary production by forming quasi-stable holes in the ice surface (Cook et al, 2010). Cryoconite holes collect allochthonous organic carbon (Telling et al, 2010), receive nutrients and cells from in-flowing meltwater (Irvine-Fynn and Edwards, 2013) and prevent the redistribution of debris for long enough for a multi-trophic ecosystems to develop (Hodson et al, 2008). And where there is an active ecosystem, carbon is cycled. The carbon potential of glaciers and ice sheets has been estimated to be equivalent to terrestrial soil systems (Anesio et al, 2009), and the cryoconite ecosystem could potentially be a large contributor to that (Cook et al, 2012). My work has begun to explore the role of Tardigrades in the cryoconite hole’s carbon cycle, a process they contribute to by oxidizing carbon stored in organic molecules within the cryoconite micro-habitat by grazing on algae and cyanobacteria. And recent data suggests that they could be a significant component in Svalbard cryoconite, particularly during the autumn months when they potentially contribute to cryoconite holes turning from a carbon sink to a carbon source with the onset of seasonal snowfall.

Although small and innocuous, Tardigrades might play a huge role in developing our understanding of the limits and origins of life. Where they exist, their role in biogeochemical cycling and microbial ecology needs to be better understood, especially in truncated glacial food webs where their top-down controls upon community ecology might be important.

To summarise, I think we should all pay homage to the space-venturing, ice-surviving, reanimating microscopic “hoover-bag”: The water-bear, the moss-piglet, the Tardigrade!
J Bartlett

 

References:

Anesio, A., Hodson, A., Fritz, A., Psenner, R. & Sattler, B. (2009). High microbial activity on glaciers: importance to the global carbon cycle. Global Change Biology. 15: 955–960.

Blatt, J., & Roces,F. (2001). Haemolymph sugar levels in foraging honeybees (Apis Mellifera carnica): Dependence on metabolic rate and in vivo measurement of maximal rates of trehalose synthesis. Journal of Exp. Bio. 204: 2709–2716.

Cook, J., Hodson, A., Telling, J., Anesio, A., & Bellas, C. (2010). The mass – area relationship within cryoconite holes and its implications for primary production. Journal of Glaciology. 51: 106–110.

Cook, J., Hodson, A., et al. (2012). An improved estimate of microbially mediated carbon fluxes from the Greenland ice sheet. Journal of Glaciology. 58:1098-1108.

De Smet, W., & Van Rompu, E. (1994). Rotifera and Tardigrada from some cryoconite holes on a Spitsbergen (Svalbard) glacier. Belg J Zool. 124: 27–37.

Everitt, D. (1981). An ecological study of an Antarctic freshwater pool with particular reference to Tardigrada and Rotifera. Hydrobiologia. 83: 225-237.

Hodson, A., Anesio, A., Tranter, M., Fountain, A., Osborn, M., Priscu, J., Laybourn-Parry, J., & Sattler, B. (2008). Glacial ecosystems, Ecological Monographs. 78: 41–67.

Irvine-Fynn, T.D.L., Edwards, A., Newton, S., Langford, H., Rassner, S., Telling, J., Anesio, A., Hodson, A.J. (2013). Microbial cell budgets of an Arctic glacier surface quantified using flow cytometry. Environmental Microbiology. 14: 2998 – 3012.

Jönsson, K. I., Rabbow, E., Schill, R. O., Harms-Ringdahl, M. & Rettberg, P. (2008). Tardigrades survive exposure to space in low Earth orbit. Curr. Biol. 18: 729-731.

Kohshima, S., (1984) A novel, cold tolerant insect found in a Himalayan glacier. Nature. 310: 225-227.

Nelson, D.R. (2001). Current status of the Tardigrada: evolution and ecology. Integrative and comparative biology. 42: 652–9.

Pasini, D., & Price, M. (2014) Panspermia survival scenarios for organisms that survice typical hypervelocity solar system impact events. European Planetary Science Congress 2014, EPSC Abstracts, Vol. 9, id. EPSC2014-68.

Brent, C., Priscu, J et al. (2014) A microbial ecosystem beneath the West Antarctic ice sheet. Nature 512:310–313.

Ramazzotti, G., & Maucci, W., (1983). Il Phylum Tardigrada. III edizione riveduta e aggiornata. Mem. Ist. Ital. Idrobiol, 411-1012 [NB: English translation is available from Dr. Clark Beasley, Biology Dept., McMurry University, Abilene, TX, USA 79697].

Renaud-Mornant, J. (1982). Species diversity in marine Tardigrada. In D. R. Nelson (ed.), Proceedings of the third international symposium on the Tardigrada, August 3–6, 1980, Johnson City, Tennessee, pp. 149–177. East Tennessee State University Press, Johnson City.

Telling, J., Anesio, A. M., Hawkings, J., Tranter, M., Wadham, J. L., Hodson, A. J., & Yallop, M. L. (2010). Measuring rates of gross photosynthesis and net community production in cryoconite holes : a comparison of field methods. Annals of Glaciology. 51:153–162.

Teramoto, N., Sachinvala, N., Shibata, M. (2008). Trehalose and trehalose-based polymers for environmentally benign, biocompatible and bioactive materials. Molecules. 13:1773-816.

Wharton, R.A., Vinyard, W.C., Parker, B.C., Simmons, G.M., Seaburg, K.G. (1981) Algae in cryoconite holes on Canada glacier in southern Victoria Land, Antarctica. Phycologia. 20: 208-211

Life on Earth’s Cold Shoulder – Film

The talented folk at the University of Derby’s Media Team have whipped up this short introduction to the fascinating world of glacier microbes. We hope it makes you question whether icy landscapes really give life the cold shoulder, or whether what appear to be lifeless zones are actually sites of abundant microbial activity!

UPDATE: We’re very proud to announce that this film received a BUFVC award in April 2015! See here for details…

I am extremely grateful to the Gino Watkins Memorial Fund, Andrew Croft Memorial Fund and Scottish Arctic Club for supporting field work in 2014. Furthermore, everyone at the Dark Snow Project are sincerely thanked for sharing field resources at S6. Thank you also to the UoD Media team, in particular Hannah Davies and Matt Howcroft, who put loads of time and effort into making this film!

For more information, see the literature in this cryoconite bibliography.

The Dark Snow Project contributed to this project by sharing their camp at S6. See their webpage at darksnow.org
We are grateful to the Dark Snow Project for sharing their camp at S6 in summer 2014. See their webpage at darksnow.org for more info.

Greenland 2014: Field Work Report

The Greenland ice sheet is the largest continuous body of ice in the northern hemisphere, covering an area of ~22million km^2. Despite appearing to be devoid of life, it is a huge reservoir of microbial biodiversity, offering many habitats for microscopic lifeforms. These microbes might play an important role in the way the ice sheet behaves, including how quickly it melts.

Greenland ice sheet melt in action: observing surface runoff in a stunning supraglacial stream (ph. Sara Penrhyn-Jones)
Greenland ice sheet melt in action: observing surface runoff in a stunning supraglacial stream (ph. Sara Penrhyn-Jones)

One particularly important habitat is cryoconite. Cryoconite refers to granular aggregations of minerals and biological material that provide microhabitats for a range of organisms, including those that use sunlight to harvest energy (autotrophs) and those that feed upon organic carbon (heterotrophs). Biological material makes cryoconite very dark, meaning it often drills down into the ice surface forming pits called cryoconite holes. We currently have a weak understanding of the bio-glaciological implications of these processes, which is why Dr’s Arwyn Edwards, Tris Irvine-Fynn and I spent the last month on the Greenland ice sheet immersing ourselves in the dark and dirty world of cryoconite.

The beautiful cryoconite at S6, Greenland ice sheet
The beautiful cryoconite at S6, Greenland ice sheet

We spent two exciting weeks in a field camp kilometres into the ice sheet, at a site known as S6, with the Dark Snow Project. These scientists were examining the links between algal growth and the darkening of the ice surface (http://darksnowproject.org/).

Dr Irvine-Fynn: out of the helicopter and onto the ice...
Dr Irvine-Fynn: out of the helicopter and onto the ice…

My primary focus was on cryoconite. I previously found that cryoconite holes widen when supplied with sediment, causing cryoconite to spread out and maintain maximal exposure to solar radiation (required for photosynthesis), whilst still being protected from the local weather and melt runoff by hiding on hole floors. This season, I looked in detail at the implications of this for biogeochemical cycling in cryoconite.

Peering into one of thousands of cryoconite holes at camp!
Peering into one of thousands of cryoconite holes at camp!

Furthermore, Arwyn and I jumped at the chance to visit a site further inland, in the accumulation zone of the Greenland ice sheet, with a shallow ice corer. A whirlwind visit saw us extract three ice cores from beneath the accumulating snow. A potentially major finding was that there was liquid water present ~1m beneath the surface – possibly an aquifer feeding the microbially active ablation zone with cells and nutrients and greatly expanding the known habitable area of the ice sheet. Such an aquifer has been identified before in Eastern Greenland, but this might be the first time it has been observed on the western coast.

Dr Arwyn Edwards (left) and me removing the first of three ice cores that struck subsurface liquid water (ph. Sara Penrhyn-Jones)
Dr Arwyn Edwards (left) and I removing the first of three ice cores that struck subsurface liquid water (ph. Sara Penrhyn-Jones)

Although we were blessed with stable, sunny conditions for most of the field season, one dramatic change in the weather reminded us how remote the site was and how uncomfortable field work can sometimes be. Drying clothes and equipment and staying warm can be challenging on a cold, continuously melting ice sheet…

The camp looking bleak as the weather suddenly changed for the worse...
The camp looking bleak as the weather suddenly changed for the worse…

Finally, Dr.s Edwards and Irvine-Fynn and I extracted from Camp Dark Snow and spent the remainder of our season working on the marginal zone, examining similarities and contrasts in cryoconite characteristics and hydrological processes between the edge and the interior of the ice sheet.

Dr Arwyn Edwards (front) and I examining large cryoconite pools near the margin on the Greenland ice sheet (ph. Sara Penrhyn-Jones)
Dr Arwyn Edwards (front) and I examining large cryoconite pools near the margin on the Greenland ice sheet (ph. Sara Penrhyn-Jones)

Now it is time to begin collating and processing the stack of data gathered in the field, and planning for the next visit – like any great field season, we have returned with many more questions and unexplained observations than we left with!

Sincere thanks go out to the Gino Watkins Memorial Fund, Andrew Croft Memorial Fund and Scottish Arctic Club for supporting my involvement in this trip. Also, to Arwyn Edwards and Tris Irvine-Fynn who were great field-buddies, supported by the Royal Society. Finally to the Dark Snow Project for sharing the field camp and logistics.