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 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.
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.
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…
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.
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).
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.