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Community of one

Genetic analysis reveals how a single species of bacterium thrives on its own three kilometers underground

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1:58pm, October 9, 2008
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A fracture deep underground in a South African gold mine holds a rare biological find — an ecological system populated by a single species of bacteria. An analysis of the bacterium’s complete genetic makeup, published October 10 in Science, reveals that the bacteria have all the tools to survive completely alone.

“This really stands one of the basic tenets of microbial ecology on its head,” says Carl Pilcher, director of the NASA Astrobiology Institute at the NASAAmesResearchCenter headquartered at Mountain View, Calif. Based on experience with other ecosystems, scientists thought that any microbial community would contain a variety of species, each specialized to grow on different nutrients. Some microbes would use nutrients found in the environment and make byproducts that other microbes could use to grow.

Not only does the newly characterized bacterium live alone, but it also appears to live independently of the sun-powered system that helps nourish all other organisms on, or in, the Earth. (Even bacteria that get their energy from chemical reactions get some nutrients indirectly from solar energy.) “This is the first pretty solid evidence that there is another source of energy life can use, and that is radioactive energy,” says Pilcher, who was not part of the team that discovered and analyzed the bacterium. The finding indicates that other rocky planets could support subsurface life that grows on a similar energy source, he says.

In recent years, DNA studies of oceans and other places where microorganisms live have revealed intensely diverse microbial communities. That trend is reversed the lower you go into the Earth’s crust. At about three kilometers deep, the Mponeng gold mine in South Africa is about as low as anyone has gone into the solid Earth.

It takes two to three hours just to descend the 2.8 kilometers to the fracture where a team of scientists discovered the community of one, says Tullis Onstott of the Indiana Princeton Tennessee Astrobiology Initiative. Onstott, who works at PrincetonUniversity, was a member of the team that filtered more than 10,000 liters of water from the deep-Earth crack to collect the bacteria.

The bacteria live in an environment with a paucity of nutrients. The microbes must rely on radiation from uranium and other minerals in surrounding rocks to split water molecules. Oxygen split from water reacts with iron sulfide minerals to create iron sulfate, which the bacteria can then eat. The water in the crack is old, having last been on Earth’s surface between 3 million and 10 million years ago. The water is also hot — about 60 degrees Celsius — and under as much pressure as at the bottom of the ocean.

Few organisms can withstand such extreme conditions. “It’s very lonely down there,” Onstott says.

The researchers knew that only a few microbes could live in such an environment, but they expected to find a simple community composed of several species occupying what’s called the MP104 fracture.

It came as surprise when Dylan Chivian of Lawrence Berkeley National Laboratory in Berkeley, Calif., and his colleagues examined DNA collected from microbes in the fracture and found that more than 99.9 percent of the DNA came from a single species of bacteria. The remaining 0.1 percent is mostly from contamination, Chivian says.

Jules Verne’s novel Journey to the Center of the Earth inspired part of the name — Candidatus Desulforudis audaxviator — the scientists gave to the newly discovered bacterium. Candidatus is a tag given to species that have not yet been grown in the laboratory. Desulfo indicates that the organism eats sulfates. The bacterium’s resemblance to a foot-long hotdog is reflected in the -rudis portion of the name. And audaxviator is Latin for “bold traveler,” from a passage in Verne’s book that translates to “Descend, bold traveler … and you will attain the center of the Earth.”

Desulforudis audaxviator has the genes needed to not only eat sulfates, but also to cannibalize other bold travelers, convert inorganic carbon and ammonia into cell-building materials and fix nitrogen. Nitrogen fixation, which the bacterium has borrowed from microbes called archaea, is an energetically expensive process, and some scientists are surprised to find the ability to do it in an organism that lives in such a nutrient-poor environment. The capability may be a relic of an earlier lifestyle that the bold traveler has not yet thrown away, or could be used in parts of the ecosystem where ammonia concentrations are low, says Adam Martiny, a microbial ecologist at the University of California, Irvine not involved in the study.

These bacteria likely reproduce very slowly, taking between hundreds to 10,000 years to replicate, the researchers report.

No one knows how long the bacteria have been in this fracture, but the researchers say it must have been long enough for the species to lose its ability to defend itself against oxygen.

Such a complete genetic toolkit for survival is an exciting find, Chivian says.

“You can have life living independently. You can pack everything you need into a single genome,” he says. “It’s exciting philosophically for that reason.”

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