Defining Life's Limits

A sulfur-rich, near-boiling hot spring. A remote rock more than a mile under Earth's surface. A bone-dry desert where it rains only once every few years. To us, such places may sound downright inhospitable. But for certain microbes--traditionally known as extremophiles--such locales can be a perfect place to live. So what are life's true limits?

That question was pondered and discussed by biogeochemists who gathered in San Diego last month for the American Chemical Society's national meeting. Attendees of "Biogeochemistry at the Limits of Habitability," a symposium cosponsored by the Division of Geochemistry and the Biotechnology Secretariat, were reminded that what we humans consider extreme can be another organism's dream.

"What we'd like to be able to do is accurately predict where life can--and cannot--exist," Everett Shock, a professor of geological sciences and of chemistry and biochemistry at Arizona State University, told C&EN. Biogeochemists could then predict where and under what conditions life might be found on other planets or at other times in Earth's history, added Jennifer Macalady, an assistant professor of geoscience at Pennsylvania State University, who coorganized the symposium with Shock.

To kick off the symposium, Shock introduced a new theoretical framework for comparing diverse environments' potential for supporting life, which he developed with geochemist Melanie E. Holland of Geotek Ltd. in Daventry, England. "Extreme values of some physicochemical variables can actually prevent life, but most 'extreme' physicochemical variables merely exact an energetic toll on organisms that inhabit that environment," Holland said in an interview. For instance, microbes living at low pH must pay the energetic price to pump protons out of their cells or to keep them out in the first place.

Shock and Holland challenged biogeochemists to define the "habitability" of so-called extreme environments, a quantity they define as the net energy available to an organism in an environment per unit time. "This requires that we try to quantify both the energy supply in a given environment and the energy demands that environment places on those who live there," Shock told C&EN. As a first step, biogeochemists must thoroughly characterize not only the physical conditions and chemistry of a given extreme environment but also the biochemical adaptations organisms have had to resort to in order to make that environment their home, he pointed out.

A NUMBER OF speakers recounted their attempts to characterize the energy supply available in various extreme environments. Barbara Sherwood Lollar, a geologist at the University of Toronto, is using isotope analysis techniques to characterize potential energy sources for life deep under Earth's surface. Just a decade ago, "it was thought that life only persisted down a couple hundred meters under Earth's surface," Sherwood Lollar said in an interview. In recent years, however, microbial communities have been discovered in underground mine sites that extend several kilometers under Earth's surface. "Debate has raged over what these microbes could be using as a food source," she said.

Sherwood Lollar previously showed that billions-of-years-old crystalline rocks in these mines release hydrogen and hydrocarbon gases. She wondered whether the H₂ might be used as a food source by microbes. On the basis of stable isotope ratio measurements, Sherwood Lollar reported that deep-dwelling microbes are indeed rapidly consuming H₂ (and CO₂) and producing CH₄. "Microbes could harness a substantial amount of energy from this reaction," she told C&EN. Sherwood Lollar and her microbiological collaborators have shown that the microbes making their homes on these deep subsurface rocks include ones related to hydrogen-consuming surface-dwellers.

A number of other researchers spoke of their efforts to tease out what organisms living in extreme environments use as food. Kenneth M. Voglesonger, a postdoc at Arizona State University, described his efforts to study the microbial colonization of nascent hydrothermal chimneys on the floor of the Pacific Ocean. Even though such just-formed chimneys spew superheated, highly acidic, mineral-rich water, a variety of microbes manage to live on their walls. On the basis of chemical analysis of water samples and the minerals found within the chimney as well as thermodynamic calculations, Voglesonger concluded that sulfate reduction would be an energetically favorable metabolic pathway for microbes living on newly formed chimneys. Microbiological analyses have confirmed that at least one type of microbe living there can reduce sulfate in vitro.

If you believe your nose, you might think that the microbes in Yellowstone National Park's hot springs are also powered by sulfur metabolism. But in this case, the nose knows nothing, according to John R. Spear, a senior research associate in Norman R. Pace's lab at the University of Colorado, Boulder. He measured several key chemical variables--including sulfate, hydrogen, oxygen, and methane concentrations; pH; and the reducing potential--in a number of hot springs in Yellowstone (Proc. Natl. Acad. Sci. USA 2005, 102, 2555). Thermodynamic modeling of these data indicates that H₂ oxidation is likely to be the main source of energy for organisms living in the pools, he reported.

ANOTHER SPEAKER, Albert S. Colman of the Center of Marine Biotechnology at the University of Maryland Biotechnology Institute, in Baltimore, described his lab's attempts to study who lives on what in the volcanic hot spring pools of Uzon Caldera in far eastern Siberia. These pools boast high concentrations of carbon monoxide, hydrogen, methane, and hydrogen sulfide, all rich sources of chemical potential energy. Colman reported results of genomic comparisons, microscopy experiments, and chemical analyses that suggest that CH₄-forming microbes and CO-consuming microbes in these pools share a symbiotic relationship: The CH₄-forming microbes also generate CO that's used by the CO-consuming microbes, while the CO-consuming bugs make H₂ that the CH₄-forming ones use to make methane.

Quantifying the energy demands that a given environment places on its residents is a far bigger challenge than quantifying that environment's energy supply, Shock pointed out. The first step is to identify adaptations that allow organisms to live under extreme conditions such as low pH or high pressure. At the meeting, Sabrina Tachdjian, a graduate student in Robert M. Kelly's lab at North Carolina State University, reported her efforts to use microarray profiling to study adaptations required for living at low pH. Sulfolobus solfataricus is a thermophilic archaeon that thrives in highly acidic environments. Tachdjian used a tiny DNA chip arrayed with all of the genes in S. solfataricus to assess which genes were turned on or off when the organism experienced a sudden drop in pH.

Tachdjian found that most changes in gene expression occurred within the first 30 minutes after the pH dropped. She reported that acidification appears to result in a general slowdown in cellular metabolism as well as an increase in production of a variety of what are likely lipid-producing and membrane proteins, including one involved in pumping protons out of the cell. "We now need to do some biochemical experiments to follow up on the hypotheses generated by microarray data," Tachdjian told C&EN.

Michael P. Thelen of Lawrence Livermore National Laboratory described efforts by a team led by Jillian F. Banfield of the University of California, Berkeley, to take the next step: measuring protein production directly. Previously, Banfield's lab reported the genome sequences of the two dominant members of a community of microbes that live in highly acidic, metal-rich water produced when pyrite-rich rocks are oxidized upon exposure to air and water. Now, Banfield's team has used mass spectrometry to quantify how much of what proteins these microbes produce. Banfield hopes that biochemical analysis of the most abundant proteins will reveal how these organisms persist at such low pH.

Also at the meeting, UC Berkeley's Ronald Amundson described attempts to determine the minimum amount of water required to support microbial photosynthesis--work carried out by postdoc Kimberley A. Warren-Rhodes at UC Berkeley and the National Aeronautics & Space Administration's Ames Research Center in Moffet Field, Calif. Warren-Rhodes surveyed for photosynthetic microorganisms in Chile's Atacama Desert, one of the driest spots on Earth. Where rainfall is absent, these microbes are rare and those that do exist may have found a way to harness the water in fog to power photosynthesis, she said.

In an interview, Shock admitted that it remains challenging to accurately define both the energy supply available in a given extreme environment and the energy demands that it places on the organisms that live there. What's more, an abundant energy supply may not be the only requirement for life in some locations--certain nutrients may be limiting, for example. Despite these potential limitations, "our theoretical framework may help scientists who wish to determine whether life could exist under particular conditions--for instance, on other planets or on early Earth," he added.