Bacteria Use Radioactive Uranium To Convert Water Molecules To Useable Energy

The discovery is a confirmed expansion of Earth's biosphere, the three-dimensional shell that encompasses all planetary life.

The research has less Earthly implications, however. It will likely fuel optimism that life exists in other deep subsurface environments, such as in groundwater beneath the permafrost on Mars.

"We know surprisingly little about the origin, evolution and limits for life on Earth," said IUB biogeochemist Lisa Pratt, who led IU Bloomington's contribution to the project. "Scientists are just beginning to study the diverse organisms living in the deepest parts of the ocean. The rocky crust on Earth is virtually unexplored at depths more than half a kilometer below the surface. The organisms we describe in this paper live in a completely different world than the one we know at the surface."

Bacteria living in groundwater or in other subsurface environments is not news. Until now, however, it was not known whether subterranean microorganisms were recent arrivals bound for extinction or whether they were permanent fixtures of an unlikely habitat. Also, many scientists have been skeptical of subsurface bacterial communities being completely disconnected from surface ecologies fed by the sun's light.

Pratt, Princeton University geomicrobiologist Tullis Onstatt and former graduate student Li-Hung Lin (the paper's lead author, now at National Taiwan University) and colleagues present evidence the bacterial communities are indeed permanent -- apparently millions of years old -- and depend not on sunlight but on radiation from uranium ores for their existence.

Coauthors of the present paper learned of a new water-filled fracture inside a South African gold mine near the Johannesburg metropolitan area and viewed it as an opportunity to study subsurface rock uncontaminated by human activities. Lin and others in the research team traveled to the mine and descended the hot, gas-choked shafts to study water slowly seeping from the crack.

The scientists sampled the flowing fracture water many times over 54 days to determine whether the community of microbes, if present, changed in composition and character, and to determine whether contamination had occurred. The researchers also examined the age of the fracture water and its chemical composition.

This fracture water contained hydrocarbons and hydrogen not likely to have been created through biological processes, but rather from decomposition of water exposed to radiation from uranium-bearing rocks.

High density DNA microarray analysis revealed a vast number of bacterial species present, but the samples were dominated by a single new species related to hydrothermal vent bacteria from the division Firmicutes. The ancient age of the fracture water and comparative DNA analysis of the bacterial genes suggests subsurface Firmicutes were removed from contact with their surface cousins anywhere from 3 million to 25 million years ago. The bacteria's rocky living space is a metamorphosed basalt that is about 2.7 billion years old. How surface-related Firmicutes and other species managed to colonize an area so deep within Earth's crust is a mystery.

Some surface Firmicutes species are known to consume sulfate and hydrogen as a way to get energy for growth. Other bacteria can then use the by-products of the Firmicutes as a source of food. The scientists found that the fracture Firmicutes are also able to consume sulfate. Firmicutes do not use radiation directly as a source of energy, however.

Radiation emanating from uranium minerals in or near the fracture allows for the formation of hydrogen gas from decomposition of water and formation of sulfate from decomposition of sulfur minerals. Hydrogen gas is highly energetic if it reacts with oxygen or other oxidants like sulfate, as the Hindenburg disaster demonstrated. Firmicutes are able to harvest energy from the reaction of hydrogen and sulfate, allowing other microbes in the fracture community to use the chemical waste from the Firmicutes as food.

In a way, Firmicutes serve the same function as photosynthetic organisms, such as plankton and trees at Earth's surface, that capture sunlight energy ultimately to the benefit of everything and everyone else. In the deep subsurface case, Firmicutes species are the producers, capturing the energy of radiation-borne hydrogen gas to support microbial communities.

Pratt is the project director of the continuation of this research, which examines deep "extremophile" subsurface environments in South African and the Canadian Arctic mines. Pratt is also the director of the Indiana-Princeton-Tennessee Astrobiology Institute (IPTAI), a NASA-funded research center focused on designing instruments and probes for life detection in rocks and deep groundwater on Earth during planning for subsurface exploration of Mars. IPTAI's recommendations to NASA will draw on findings discussed in the Science report. For more information about IPTAI visit: http://www.indiana.edu/~deeplife/.

Tullis Onstott (Princeton University), Lisa Pratt and graduate student Eric Boice (IU Bloomington), Li-Hung Lin and Pei-Ling Wang (National Taiwan University), Douglas Rumble (Carnegie Institution of Washington), Terry Hazen, Gary Andersen and Todd DeSantis (Lawrence Berkeley National Laboratory), Duane Moser (Desert Research Institute), Barbara Sherwood Lollar (University of Toronto), Dave Kershaw (Mponeng Mine, South Africa) and Johanna Lippmann-Pipke (GeoForschungsZentrum Potsdam, Germany) are contributors to the research. It was supported by grants from NASA, the National Science Foundation and several other entities.