Wednesday, March 2, 2011

Bold Traveler

One of my favorite television series is Life on Earth, produced by David Attenborough. Every episode seemed to feature him walking across one of the Dry Valleys of Antarctica, or the Atacama desert, or an iceberg, or solfatara. After noting how hostile the area was, Attenborough would turn over a rock and point at a green smudge or a tiny insect, and in his plummy British accent say “And yet…even this harsh environment, life persists!” For champions of endurance, though, Attenborough should have pointed to microbes. As a harsh environment, it’s hard to beat hot rocks nearly three kilometers underground—but microbial life doesn’t just persist there, it seems to thrive.

Interest in life deep beneath the Earth’s surface has been growing in recent years. There was considerable surprise when deep-drilling projects in the 1980’s revealed that oceanic basalts held diverse communities of Bacteria and Archaea. Because of the way these basalts form, we could figure out how old they were. Amazingly, rock that had been buried for millions of years carried millions and sometimes billions of microbial cells. Microscopic analysis using dyes that only stain living cells showed that the majority of these cells were alive, although living veeeery slowly. These observations stimulated further questions—in fact, the two basic questions asked by all environmental microbiologists: who are these guys, and what are they doing?

“Who is there” is easily answered in this day and age by DNA sequencing. Since Bacteria and Archaea are generally identified on the basis of ribosomal RNA sequence, DNA was extracted from these rock samples and probed for the genes encoding ribosomal RNA. These genes could be sequenced and the results would show “who” lived in young (only tens of thousands of years old) oceanic basalts. The answer is somewhat surprising. The Archaea generally have a reputation as “extremophiles,” capable of living in the harshest environments. They also are about half of the organisms found in the deepest oceans. However, in young oceanic basalts, they are only 10% of a surprisingly diverse population. In fact, there seems to be twice the diversity of bacterial species in the young basalts than in the surrounding seawater.

Probing of older basalts showed that as the environment got harsher, diversity decreased. Drilling 1600 meters beneath the ocean floor (into rocks that were deposited over 100 million years ago), researchers found an environment with temperatures ranging from 60 to 90 degrees Celsius, but with a million cells per gram of rock. These cells were definitely alive. However, unlike the younger basalts, the diversity of life sustained by these deep rocks was very low. Generally, only a few types were found, and they were evenly divided between anaerobic Bacteria and methanogenic Archaea. So there seemed to be a trend: deeper and older meant fewer cells and less diversity.

The current record for human curiosity in this subject was established in 2008. In this case, curiosity was helped by greed, as the scientists gained access to a South African gold mine and sampled the water percolating through porous rocks 2,800 meters below the surface of the earth. Conditions there are beastly—a temperature of 60°C (140°F—give a thought to the humans who work there!). Worse, there’s very little energy available. We humans get energy by burning carbon compounds in oxygen; the bacteria living in ocean sediments get energy by burning carbon compounds in sulfates. But in these deep rocks, it seems at first glance that there’s nothing to burn.

“And yet, even here in this harsh environment, life persists!” Not much life, though, and no diversity. The researchers didn’t actually observe any cells—they simply collected DNA. Although this DNA was somewhat similar to that of known types of bacteria, it was unique—enough so that the researchers postulated that it belong to a previously unknown organism, which they named Desulforudis audaxviator. Amazingly, there is no diversity in this environment. They sampled half a million pieces of DNA from this environment, and 99.96% of it came from D. audaxviator. They found essentially no other DNA in their samples. It appears that D. audaxviator—it means “bold traveler”—lives alone in the rocky depths.

We are used to a “web of life,” with organisms interconnected by chemistry and energy: up here, the plants take light and carbon dioxide to make glucose, while we eat the plants to make carbon dioxide, and so on. There are similar cycles for nitrogen, sulfur and other elements, and ultimately, all of these cycles are powered by energy from the sun. Bold traveler lives by itself, depending on no one and feeding no one, a situation unique in my experience in biology. The researchers’ analysis of Bold traveler’s genes show how it can be a one-species ecosystem. It’s able to take in carbon dioxide and make sugar (instead of photosynthesis, it uses chemosynthesis, a light-independent process). It can also “burn” that sugar, using sulfate instead of oxygen, and get energy. It can fix nitrogen, the same way that the bacteria that live in bean plants do. It contains all the element cycles in itself.

If a solo ecosystem is surprising, the energy that probably powers this ecosystem is amazing. We can tell by its genes that Bold traveler burns its fuel using sulfate in place of oxygen—it has the genes for it. But what is less clear is the nature of the fuel it uses. The fuel may be sugar, but there’s very little of that available in the deep rocks. Its genes suggest that Bold traveler burns hydrogen as its fuel. You might reasonably expect hydrogen to be rare in these rocks—it’s a light gas, and would want to be up in the air. But there is water in these rocks, and there is another critical thing: energy.

You may have seen an apparatus that uses electricity to break water into its constituents: electrodes are dipped into water, and a fairly powerful voltage results in oxygen coming off of one electrode, hydrogen off the other. There are no electrodes in the rocks deep underground, but there is energy: the radioactive decay of elements such as thorium and uranium is able to pry hydrogen away from oxygen. Although we don’t know this for sure, we can calculate that the amount of radioactivity present in these rocks is sufficient to keep cells such as Bold traveler alive. So, our best guess is that Bold traveler is, indirectly, nuclear powered: radioactive decay produces hydrogen from water, and Bold traveler burns that hydrogen using sulfate in the rocks it lives in. Unlike just about every other organism we’ve ever seen, Bold traveler is completely independent of the sun.

This all sounds freaky, and for one trained in the biology of “normal” organisms, rather suspect. But what is normal? If normal is what the majority does, that Bold traveler may be normal, and we are the freaks. All the life we are used to—all the birds and trees and people and whales, all the microbes that live in the soil and oceans—are just the thinnest of films on the surface of the earth. The biosphere we know is at best a few meters thick on a globe twelve and a half million meters across. Sure, the life we know may grow to great densities in this environment, but it is a tiny environment. Now consider bold traveler and its fellows: their environment is poor, but thousands of times larger than ours. A simple calculation shows that the majority of microbial life--perhaps the majority of all life--persists in this harsh environment. It's enough to make me envision a microbial Attenborough, trudging through a lush rainforest or fertile farmland, saying "...and yet, even in this harsh environment, life persists!"

By the way, that name—D. audaxviator—is kind of a joke. It refers to Jules Vernes Journey to the Center of the Earth. The heroes of the story are guided by instructions, in Latin, addressed to the “bold traveler”, or audax viator.

Dylan Chivian et al. (2008). Environmental Genomics Reveals a Single-Species Ecosystem Deep Within the Earth. Science 322: 275-278.

Erwin Roussel et al. (2008). Extending the Sub-Sea-Floor Biosphere. Science 320: 1046.

Cara M. Santelli et al (2008). Abundance and Diversity of Microbial Life in Ocean Crust. Nature 453: 653-657.

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