Genome sequencing of cells plucked from marine sediments reveals metabolic details for two abundant lineages of Archaea. These microorganisms may play a key part in breaking down protein buried deep inside Earth. See Letter p.215
Vast communities of single-celled organisms reside in a microbial purgatory deep below Earth's surface. They are known as the intraterrestrials. Bounded from below by the inhospitable temperature of Earth's interior, intraterrestrials face a chronic limitation of food-derived energy1 because they are far removed from sunlight-driven productivity. Once thought barren of life, their subsurface realm is now recognized as a varied habitat influenced as much by geological processes as by the biosphere (Fig. 1). All three domains of life — Bacteria, Eukarya and Archaea — are represented there, as are the viruses that infect them. On page 215 of this issue, Lloyd et al.2 present genome sequences of four intraterrestrial archaea. The sequences shed light on the history of this enigmatic domain, and suggest that the groups that these organisms represent contribute to the degradation of proteins in sediments blanketing the ocean floorFootnote 1.
To arrive at these findings, Lloyd and colleagues harvested sediment from the upper fringe of the subsurface biosphere, just a few metres beneath the sea floor in a Danish bay. They separated individual cells from the sediment before sequencing the cells' DNA and reconstructing their genomes by aligning millions of overlapping DNA fragments. This provided incomplete reconstructions of genomes for four archaeal organisms that represent two evolutionary lineages (three of the four are near relatives and one is a distant cousin). The estimated capture of genomic content, ranging over 32–70%, was sufficient to identify each organism's evolutionary placement and core metabolisms but not to rigorously exclude any specific genetic capability. The authors analysed the genomes to identify specific genes and their functions, reconstruct metabolic networks and ascertain evolutionary relationships with other organisms.
Our current ability to pluck an individual cell from the environment and sequence most of its genome is a far cry from the manual 'fingerprinting' with sheets of cellulose acetate paper used by the late biologist Carl Woese in the 1970s to first recognize the archaeal domain. Deciphering the evolutionary history of microbes in the face of such technological advances requires iterative refinement. Some bacterial lineages evolve so rapidly that attempting to resolve their deep evolutionary history may prove futile3, and the loss of superfluous genes in organisms that live in symbiosis with others, such as some hyperthermophilic archaea4, may obscure traditional metrics of relatedness. Nonetheless, the evolutionary distinction between Bacteria and Archaea remains firm5. And because the organisms sequenced by Lloyd and colleagues have evolved a lifestyle suited to the subsurface environment and paced to change on geological timescales, they should provide a window on the early stages of microbial evolution. Indeed, the genomes reveal ancient evolutionary splits, perhaps to the phylum level for one lineage, and our understanding of these relationships is sure to develop further. We can rely on one certainty, though: the name tags presently assigned to these groups — the miscellaneous crenarchaeotal group and the marine benthic group-D — will soon be replaced with something of Latin etymology.
The authors' comparative analysis of these four genomes points to a common metabolic strategy, which in turn suggests a potentially important role for these organisms and their relatives in the biosphere at large. The core metabolism for both lineages seems to involve the breakdown of proteins for energy generation. Apart from some biochemical differences, it seems that all four archaea do this by breaking apart proteins outside the cell, transporting the resulting peptides into the cell, metabolizing them and conserving the derived energy by pumping cations out of the cell. The portion of metabolism that occurs outside the cell may result from an adaptation to confinement between grains of sediment; using extracellular enzymes may provide access to proteinaceous 'geomolecules' that are too large to enter the cell, with the added bonus that the enzymes remain in the local environment. The diet of one lineage seems to include D-amino acids, which are enriched in the cell walls and spores of some bacteria and so are deposited to and synthesized within the subsurface biosphere6. Thus, it seems that members of these lineages decompose protein deposited during sedimentation or formed in the subsurface, including that released by the decay or dismemberment of bacteria and their spores.
The genomes also reveal a dearth of genes that might couple their metabolism to respiration. This intriguing finding is consistent with the archaea using a fermentative metabolism. However, the paucity of protein substrates in the subsurface environment may inhibit the classic Stickland-type amino-acid fermentation7 and force these intraterrestrials into syntrophic, or 'cross-feeding', relationships with other organisms amenable to accepting their waste products8. Although some of the metabolic details remain unclear, the high-protein diet proposed for these intraterrestrials may be of broad importance, as it implies that their metabolism may release bound nitrogen that is otherwise recalcitrant in marine sediments.
With a globally distributed population that could be of the order of 1027 individuals (based on a relative abundance of these organisms of approximately 0.4% in a total cellular abundance in the sub-sea-floor sediment9 of 2.9 × 1029), it is hard to argue with the evolutionary success of these intraterrestrial archaeal lineages or to marginalize them as relicts of bacterial evolution gone awry. Although circumstantial, the evidence presented by Lloyd et al. suggests that these lineages persist despite chronic calorie restriction. Such a lifestyle is consistent with the theory that adaptations to manage chronic energy stress are hallmarks of the ecology and evolution of the archaeal domain10.
Lloyd and colleagues' results are exciting not only because they raise questions about the ecology, evolution, metabolism and biogeochemistry of intraterrestrial life, but also because they point to directions that might provide answers. For example, the archaeal genomes hold clues that will guide strategies for cultivating these organisms, and isolation in pure culture would enable studies of their evolution, biochemistry and physiology. Similarly, knowing the genomic content of these archaea will allow environmental surveys and experiments to probe their genetic variability, the abundance and content of their gene transcripts, their protein machinery, their natural levels of metabolic activity and their population dynamics. We are clearly just scratching the surface of the subsurface.
*This article and the paper2 under discussion were published online on 27 March 2013.
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