The cold case of Deep Lake

Conditions in an isolated lake in eastern Antarctica are so hostile that almost nothing can survive there. For a small group of extremophile microbes, there’s nowhere else they’d rather be. 

 Illustration by Olivia Baenziger

Illustration by Olivia Baenziger

Deep Lake in East Antarctica is one of the least productive ecosystems on earth, but it’s also one of the most remarkable. Its waters are 10 times saltier than the ocean, rivaling even the Dead Sea. This high salinity keeps the lake liquid, despite water temperatures reaching -20ºC at its deepest point. This is a habitat where most organisms have failed to make their mark.

On the shores of the lake are century-old carcasses of penguins and seals, their preserved bodies pickled stiff by the high salt and cold.

“We still see penguins occasionally going into the water,” said Professor Ricardo Cavicchioli, an environmental microbiologist at University of New South Wales. “It’s not a nice environment for them; it’s much colder than the ocean.”

But much smaller life forms have carved out a place for themselves here. Deep Lake is host to only four species, three of them members of Archaea, a domain of life that has constantly unsettled existing scientific paradigms.

 
  The cold, vibrant waters of Deep Lake in East Antarctica.  Ricardo Cavicchioli (used with permission)

The cold, vibrant waters of Deep Lake in East Antarctica. Ricardo Cavicchioli (used with permission)

 

Archaea first shook up biology 25 years ago, when they were classified as the third domain of life alongside Bacteria and Eukarya. Previously grouped with bacteria, they are remarkable taxa that can exist in an extraordinary range of temperatures, from -20ºC to 122ºC. A notable faction of the Archaea are extremophiles: species that thrive in environments characterised by temperature, salinity or acidity extremes. From deep-sea hydrothermal vents to acidic hot springs to the water core of nuclear reactors — where other organisms fear to tread, extremophiles are quite comfortable to call it home.

Deep Lake is no exception. The lake is located in an Antarctic oasis — the Vestfold Hills, one of the few ice-free areas on the otherwise icy continent.  The landscape is perforated with hundreds of inland lakes, a legacy from 3500 years ago when the ice mass receded. As Antarctica rose above sea level, it created a coastal area with pockets of stranded seawater. Each inland lake, isolated for thousands of years, has developed unique ecosystems with their own evolutionary trajectories, each one like a time capsule. But Deep Lake is unusual. It sits 55 metres below sea level, with water salinity only increasing as it gets deeper.

 
  Deep Lake is located in the Vestfold Hills region of East Antarctica. Map: Australian Antarctic Data Centre.  Satellite image: Landsat Image Mosaic of Antarctica (used with permission)

Deep Lake is located in the Vestfold Hills region of East Antarctica. Map: Australian Antarctic Data Centre. Satellite image: Landsat Image Mosaic of Antarctica (used with permission)

 

Deep Lake’s isolated geography and environmental conditions helped to shape its microbial community, said Prof Cavicchioli, who has led multiple Antarctic expeditions to study microbial communities in these lake systems. In particular, the Deep Lake community is populated by psychrophilic haloarchaea, cold-loving microbes that require high salt concentrations for growth.

“The organisms that were in the lake then started to evolve to that increasing salinity, seeded by the marine population that was trapped in the lake and selected by the cold and the high salt,” said Prof Cavicchioli. “The ones that we now see are the winners.”

The most recent Deep Lake expedition in 2013 was the longest and most extensive yet for Prof Cavicchioli’s research team, spanning 18 months. They worked from mobile workstations constructed on the shores of the lake. For the first time, the Deep Lake biosphere was sampled through a complete annual cycle, including over winter.

 
  Researchers conducted their research from mobile work shelters on the Deep Lake shoreline.   Photos from 2008 expedition.  Ricardo Cavicchioli (used with permission)

Researchers conducted their research from mobile work shelters on the Deep Lake shoreline. Photos from 2008 expedition. Ricardo Cavicchioli (used with permission)

 

The scientists collected water samples from various depths, which were passed through a series of filters to separate organisms according to size. The samples were then transported back to Sydney for metagenomic analysis.

Metagenomics is a powerful form of DNA sequencing. First, the biological material is lysed, a chemical process that breaks open the cell membrane to release all its cellular components, including protein and DNA fragments. From this multi-species jumble of cell fragments, metagenomics can painstakingly interpret and reconstruct each fragment using metagenomic libraries into complete genetic sequences.

The advent of DNA sequencing technology has transformed the field of environmental microbiology, said Prof Cavicchioli. “Your ability to ask questions and discover things is completely revolutionised”. 

The result is a rapid and detailed view of the microbial community in all its diversity. This is far more useful than ‘cultivation-based methods,’ as these extremophiles reside in conditions that are impossible to replicate in the laboratory. 

A similar approach was previously used to study microbial ecology in hydrothermal vents, but Prof Cavicchioli hoped it would translate to the cold biosphere, a world away from the volcanic heat and crushing pressure of the deep sea. Indeed, metagenomics has revealed the ecology, adaptive biology and other properties of psychrophilic microbes in the Antarctic inland lake. 

 
  After taking samples from Deep Lake (left), the water undergoes filtration (right) prior to metagenomic analysis back in Sydney.   Photos from 2008 expedition.  Ricardo Cavicchioli (used with permission)

After taking samples from Deep Lake (left), the water undergoes filtration (right) prior to metagenomic analysis back in Sydney. Photos from 2008 expedition. Ricardo Cavicchioli (used with permission)

 

Diversity in Deep Lake is extremely low. Metagenomic results from a 2008 expedition revealed that three species of haloarchaea make up the bulk of the biosphere, alongside a species of green algae that grows on the surface waters. The algae are the primary producer and the only organism that contributes organic matter to the system, which the haloarchaea are quick to appropriate. This is a co-existence unique to Deep Lake.

Genomic analysis has revealed that each Deep Lake haloarchaea species has distinctive metabolic pathways and behaviour indicative of niche adaptation, meaning that they reside in different habitats within the lake. Each species has its own preference for different depths; some consume protein in the water, while others consume sugars such as glycerol, a byproduct produced by the green algae.

The most dominant haloarchaeal species is tADL, whose behaviour flexes with the Antarctic seasons. During summer, it congregates in shallower and sunnier parts of the lake using gas vesicles ‒ internal cellular balloons that provide tADL with buoyancy as it migrates towards the surface.  

The annual sunlight cycle in Antarctica is basically one extremely long day. In summer, the continent experiences continuous sunlight over a single protracted period, before descending gradually into complete darkness over winter. All organisms need to adapt to these polar conditions: light-dependent species must use light effectively during summer, but still be able to function during darker periods. Around Deep Lake, the ambient temperatures can reach -40ºC during winter months. The air is so cold that researchers had to take special procedures to prevent the water from freezing as it was removed from the lake.

 
  Penguin carcasses on the shores of Deep Lake, preserved by the salt and cold.  Ricardo Cavicchioli (used with permission)

Penguin carcasses on the shores of Deep Lake, preserved by the salt and cold. Ricardo Cavicchioli (used with permission)

 

From their genomes, you can identify evolutionary adaptations used by haloarchaea to colonise their environment. For the Deep Lake community, life proceeds in slow motion. In laboratory conditions at -1°C (the temperature at the surface of the lake), the haloarchaea divide only six times per year, a glacial pace compared to E. coli, which divides every 20 minutes.

However, in the close quarters of Deep Lake, a very distinctive evolutionary element is at play. The Antarctic haloarchaea are quite promiscuous, engaging in a high rate of gene swapping across the lake’s species. This bartering of genetic information between distinct species is an infrequent occurrence in other environments. However, despite this genetic exchange, the microbial community does not homogenise; haloarchaeal species still retain their unique genetic identity.

The reason may lie in their environment. In a habitat that offers very limited options, each species co-exists in their respective ecological niches. Each haloarchaea is partitioned off by what seem to be evolutionary barriers, such as their optimal temperatures and their metabolic pathways. 

As isolated as Deep Lake is, Prof Cavicchioli emphasises that it is a microcosm that represents the importance of maintaining and preserving microbial diversity on a much larger scale, especially their contribution to the nutrient cycle. “The world is largely microbial, and they perform critical roles,” he said. “Environmental microorganisms perform roles in life that no other organism can do.”

Cold environments below 5ºC, including the ocean, represent a vast bulk of the planet, around 85%, and from an anthropocentric viewpoint it is far too cold for us to colonise. However, these environments are dominated by microbes. In fact, 95% of the ocean’s biomass is microbial.

To ask ecologically relevant questions about extremophiles, we need to remember that the word ‘extreme’ is used from an anthropocentric standpoint. Extremophiles were named by humans and thus defined by what are considered extreme conditions from our perspective. Transplant an extremophile usually content in the heat of the hydrothermal vent to room temperature, and the sheer shock would probably kill it. The terms ‘extreme’ and ‘stress’ are relative; extremophiles are in their natural state and thrive within their own specialties and ecological niches. 

Recent attention has turned to cellular components of extremophilic archaeal cells that might be appropriated for biotechnology or industrial purposes.  Extremophile enzymes that can withstand high temperature processes have an indispensable presence in laboratories. Taq polymerase and Pfu DNA polymerase, two essential enzymes in polymerase chain reaction, a technique that revolutionised forensic science and hereditary testing, have their origins in heat-loving extremophiles

 
  Polymerase chain reaction, an important technique in molecular biology, was developed using enzymes from extremophile organisms.   Karl Mumm/Wikimedia Commons  (CC BY-SA 3.0)

Polymerase chain reaction, an important technique in molecular biology, was developed using enzymes from extremophile organisms. Karl Mumm/Wikimedia Commons (CC BY-SA 3.0)

 

The cold-adapted enzymes of psychrophilic Antarctic haloarchaea may also hold potential in low-temperature industrial applications. Enzymes from other psychrophilic species have already been considered, as they minimise the heat requirement and offer a more efficient biological solution than existing alternatives. There is currently research in using Antarctic haloarchaeal enzymes to clean water filtration systems. Using psychrophilic enzymes will bypass the need to use harsh chemicals such as bleach or sodium hydroxide. 

The word Archaea literally means ‘primitive beginnings.’ When the third domain of life was named as such, it suggested an archaic organism, proliferating in acidic ponds and boiling waters that mirror the primordial soup at the very origin of life on earth. 

However, rather than existing in the past, archaea offer insights into the present and future of evolution. These organisms have always strayed from our mainstream understanding of life: they forced us to re-draw the tree of life, and to rethink the extremes at which life can survive. While we puzzle over their unique biology, in this Antarctic lake exiled from the ocean thousands of years ago, the haloarchaea continue to thrive and persist, steadfast, right in their element. And there is nowhere else they’d rather be. 

Edited by Andrew Katsis and Ellie Michaelides, and sponsored by Andrew Waddington