Environmental genomics reveals single-species ecosystem deep within the Earth
LAS VEGAS – The October 10 issue of Science will feature DRI researcher Duane Moser’s contribution to more than 10 years’ work by an international team that presents the clearest view yet of Earth’s deep continental biosphere.
“For years in South Africa we kept detecting the same unusual microorganism in the deepest, hottest, most pristine samples,” Moser said. “Deeper than about two kilometers, it always dominated; but otherwise, had never been seen before. Was it real? Was it a contaminant? We never really knew for sure. The complete genome introduced today holds the answers to many of these questions. We still can’t grow the organism in the lab, but we have all of its genes: its entire genetic history and all of its tools for living at boundary between biosphere and lithosphere.”
Moser oversaw field operations and sample collection covering much of the six-year Witwatersrand Deep Microbiology Project in South Africa. In this capacity, he helped coordinate the preliminary microbial and geochemical analysis that set the stage for the present study. The current report, led by collaborator Dylan Chivian and colleagues from Lawrence Berkeley National Laboratory, is the latest in a series resulting from access to precedent-setting samples first obtained by Moser and his then postdoctoral advisor, T.C. Onstott of Princeton in 1997.
The samples of ancient fracture water, upon which this paper and a prior related work, also published in Science (Lin et. al, 2006) are based, were collected in 2003 from the deepest mine in the world, AngloGold Ashanti’s Mponeng Mine near Carletonville, South Africa. Here, pristine fracture water was obtained from a large water-bearing fault deep within undisturbed rock via an exploratory borehole at a depth of 2.8 kilometers (1.7 miles). In order to obtain sufficient DNA to enable community genomics on these very low biomass samples, 5,600 liters of water were filtered underground.
This work represents the first application of the emerging technology of environmental genomics to samples from the deep subsurface. It also provides one of the first complete genomes from an uncultivated organism from any habitat. These feats were possible due the unprecedented simplicity of the microbial community at this site. Multiple lines of evidence were utilized to confirm that the deep fracture was functionally (> 99.9%) a single-species ecosystem: the first ever described. This remarkable assertion was supported through a comprehensive examination of the gene complement of the inferred organism (introduced as Candidatus Desulforudis audaxviator).
An examination of the 2157 predicted genes present on the 2.35 million base-pair genome revealed all processes necessary for life, including energy metabolism, carbon fixation and nitrogen fixation. The genome also encodes functions which confirm earlier hypotheses by the group concerning how a deep, slow biosphere might operate in isolation from solar inputs by utilizing the products of natural subsurface radioactivity. In particular, D. audaxviator’s predicted ability to respire sulfate enables it to utilize the most favorable energy resource in its habitat. Many of the genes present derive from distantly-related organisms, suggesting that D. audaxviator has preserved the essential functions of multiple long-extinct community members within a single genome.
“We are taught in school that all life is connected: that energy for the biosphere always comes from the sun,” Moser said. “The results of a growing body of evidence, however, suggest that life is not confined to a thin lighted veneer at the surface, but rather may populate the vast uncharted interior volume of the continents. This other biosphere appears to persist in isolation from our familiar photosphere by reliance upon purely geological resources. If this model holds up, it is entirely possible that a large proportion of life on Earth remains to be discovered deep underground. The genome being released today represents an opportunity to examine in unprecedented detail whether such a lifestyle is possible.”
Collectively, the completed genome of D. audaxviator (which translates to “bold traveler”) reveals a uniquely independent microbial lifestyle, well-suited to long-term isolation deep within the Earth’s crust, and that alternative biospheres are possible on Earth and possibly elsewhere in the solar system.