An ecosystem of one in the depths of a gold mine

Most of the planet's ecosystems are made of a multitude of different species, rich tangles of living things all interacting, competing and cooperating in order to eke out an existence. But not always - in South Africa, within the darkness of a gold mine, there is an ecosystem that consists of a single species, a type of bacteria that is the only thing alive in the hot, oxygen-less depths. It is an ecosystem of one, living in complete isolation from the Sun's energy.

This incredible and unique habitat was discovered by Dylan Chivian from the Lawrence Berkeley National Laboratory, leading a large team of scientists from 15 institutes. The group was interested in studying extremophiles, species of bacteria that live in the planet's most inhospitable of conditions - in this case, the rocks of the Earth's crust. At depths of a kilometre or more, bacteria face unique challenges that their counterparts on land or sea do not, including high 60C temperatures and a lack of sunlight, oxygen and nutrients.

The species that can beat these challenges are interesting to biologists because they provide insights into how life can persist on the edge of existence and, potentially, on other planets. To find such species, Chivian's team of bacteria-hunters did their work in a series of mines in South Africa's Witwatersrand basin. In one venture, they collected over 5,000 litres of water that had pooled in cracks in the rock almost 3km deep.

They used a technique called 'metagenomics' to extract and analyse all the DNA from the sample. Metagenomics allows scientists to study the hidden worlds within any given habitat and to identify the multitude of bacteria and other micro-organisms that live there. Usually, the technique gives an interesting overview but would never be able to provide a complete census of the local species. But in the deep water, Chivian found a surprise. All the DNA belonged to a single species of bacteria, which they named Candidatus Desulforudis audaxviator.

The name is an apt one; "audaxviator" means "bold traveller" and comes from a quote from Jules Verne's novel Journey to the Centre of the Earth. The species' genes have been isolated from other crust samples before but this is the first time that it has been found in total isolation. And to a large extent, this community of one shares a single genome. The population has a staggeringly low level of genetic diversity. Among the 2.3 million base pairs that make up its genome, only 32 displayed mutations that cropped up more than once. D.audaxviator is not one for individuality.

Chivian thinks it unlikely that there are any other microbial hangers-on in the mine, for the methods he used have successfully isolated DNA from other microbes in the past. About 0.1% of sequences he identified didn't fit into the main genome but Chivian thinks that these came from contaminating species, most of which had been picked up in the lab and others which came from rocks higher up in the mine. If there are other species sharing the same space as D.audaxviator, they make up at most about 0.035% of the bacteria in the water and would be outnumbered by the dominant species by at a factor of 5,000.

D.audaxviator's genes revealed its abilities as well as its identity, and these support the idea that it is the sole occupant of the mine's depths. The bacterium has all the metabolic abilities it needs to live an independent existence. It gets all the nutrients it needs from the minerals in the surrounding rocks, using sulphate ions in place of oxygen and getting nitrogen and carbon from ammonia and carbon dioxide dissolved in the surrounding water. It can even get an extra boost of nutrients by recycling dead cells of its own kind.

It can form hard coats called endospores to protect it from dehydration or toxins, it has genes that allow it to sense nutrients, and it can create the components of flagella - whip-like tails that allow bacteria to move around. In fact, one of the only talents it lacks in comparison to other bacteria is the ability to deal with the dangerous chemical byproducts of oxygen metabolism. But then again, it hardly needs such a skill in an environment devoid of the usually essential gas.

Many extremophiles survive by slowing their reproductive abilities, taking hundreds or thousands of years to divide, and paring down their genomes to just the bare necessities. But not D.audaxviator - it retains a genome size that is comparable to other free-living bacteria. Many of these abilities are the result of proteins that it has freely pilfered proteins from another kingdom of micro-organisms that is rife with extremists - the Archaea. These genetic loans, taken out before it moved into the gold mine, are the key to its success in this most inhospitable of environments.

Reference: D. Chivian, E. L. Brodie, E. J. Alm, D. E. Culley, P. S. Dehal, T. Z. DeSantis, T. M. Gihring, A. Lapidus, L.-H. Lin, S. R. Lowry, D. P. Moser, P. M. Richardson, G. Southam, G. Wanger, L. M. Pratt, G. L. Andersen, T. C. Hazen, F. J. Brockman, A. P. Arkin, T. C. Onstott (2008). Environmental Genomics Reveals a Single-Species Ecosystem Deep Within Earth Science, 322 (5899), 275-278 DOI: 10.1126/science.1155495

Image: Greg Wanger and Gordon Southam