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Bacteria stir debate about 'shadow biosphere'

By Marc Kaufman
Washington Post Staff Writer
Friday, December 3, 2010; 9:12 PM

All life on Earth - from microbes to elephants and us - requires the element phosphorus as one of its six components.

But now researchers have discovered a bacterium that appears to have replaced that life-enabling phosphorus with its toxic cousin arsenic, raising new and provocative questions about the origins and nature of life.

News of the discovery caused a scientific commotion this week, including calls to NASA from the White House asking whether a second line of earthly life has been found.

A NASA press conference Thursday and an accompanying article in the journal Science said the answer is no. But the discovery opens the door to that possibility and to the related existence of a theorized "shadow biosphere" on Earth - life evolved from a different common ancestor from all we've known so far.

"Our findings are a reminder that life-as-we-know-it could be much more flexible than we generally assume or can imagine," said Felisa Wolfe-Simon, 33, the biochemist who led the effort.

Prompted by debate about the possible existence of a shadow biosphere, Wolfe-Simon set out specifically to see whether microbes that lived in California's briny, arsenic-filled Mono Lake naturally used arsenic instead of phosphorus for basic cellular functions, or were able to replace the phosphorus with arsenic.

She took mud from the lake into the lab and began growing bacteria in Petri dishes. She fed them sugars and vitamins but replaced phosphate salt with arsenic until the surviving bacteria could grow without needing the phosphates at all.

Her research found that some of the bacteria had arsenic embedded into their DNA, RNA and other basic underpinnings.

"If something here on Earth can do something so unexpected - that breaks the unity of biochemistry - what else can life do that we haven't seen yet?" said Wolfe-Simon, a NASA Astrobiology Research Fellow and member of the National Astrobiology Institute team at Arizona State University.

"This is different from anything we've seen before," said Mary Voytek, senior scientist for NASA's program in astrobiology, the arm of the agency involved specifically in the search for life beyond Earth and for how life began here.

"These bugs haven't just replaced one useful element with another; they have the arsenic in the basic building blocks of their makeup," she said. "We don't know if the arsenic replaced phosphorus or if it was there from the very beginning - in which case it would strongly suggest the existence of a shadow biosphere."

Theoretical physicist and cosmologist Paul Davies, director of the Beyond Center at Arizona State and a prolific writer, is a co-author on the new Science paper. He had been thinking about the idea of a shadow biosphere for a decade and had written a paper on it in 2005. The same year, philosopher and astrobiologist Carol Cleland and biochemist Shelley Copley, both of the University of Colorado at Boulder, teamed up to publish on the subject. Both asked why nobody was looking for life with different origins on Earth, and Cleland coined the phrase "shadow biosphere."

At a Beyond Center conference four years ago, Wolfe-Simon, then in her late 20s, proposed a way to search for a possible shadow biosphere, and it involved Mono Lake and its arsenic.

"We were kicking vague ideas around, but she had a very specific proposal and then went out and executed it," Davies said. "It defies logic to think she found the only example of this kind of unusual life. Quite clearly, this is the tip of a huge iceberg."

All life as we know it contains six essential elements - carbon, oxygen, hydrogen, nitrogen, sulfur and phosphorus - that have qualities that make them seemingly ideal for their tasks. A form of phosphorus, for instance, is near perfect for building the framework for the DNA molecule, and another form is crucial to the transfer of energy within cells.

These forms of phosphorus are well suited for their job because they are especially stable in the presence of water. Arsenic is not, and that fact is one that raises concerns for some researchers familiar with the Mono Lake bugs.

Chemist Steven Benner of the Foundation for Applied Molecular Evolution in Florida has been involved in shadow biosphere research for several years, and spoke at the NASA unveiling of Wolfe-Simon's work. He says that the Mono Lake results are intriguing - "I do not see any simple explanation for the reported results that is broadly consistent with other information well known to chemistry" - but he says they are not yet proved. A primary reason is that arsenic compounds break down quickly in water while phosphorus compounds do not.

His conclusion: "It remains to be established that this bacterium uses arsenate as a replacement for phosphate in its DNA or in any other biomolecule." The tests to make a more final determination, he said, are complex but available.

The paper and its results have created an excitement reminiscent of the 1995 announcement at NASA headquarters of the discovery of apparent signs of ancient life in a meteorite from Mars found in Antarctica. That finding was central to establishing the field of astrobiology, but was also broadly challenged and a scientific consensus evolved that the case for signs of life in the meteorite had not been proved.

The Mono Lake discovery highlights one of the central challenges of astrobiology - knowing what to look for in terms of extraterrestrial life. While it remains uncertain whether the lake's microbes represent another line of life, they show that organisms can have a chemical architecture different from what has until now been understood to be possible.

"One of the guiding principles in the search for life on other planets, and of our astrobiology program, is that we should 'follow the elements,' " said Ariel Anbar, an ASU professor and biogeochemist. "Felisa's study teaches us that we ought to think harder about which elements to follow."

Mono Lake was selected as a work site by Wolfe-Simon because it is highly unusual and had been well studied by other scientists trying to answer different questions.

The lake receives runoff from the Sierra Nevada mountains, which have relatively high concentrations of arsenic. When the water arrives at Mono Lake, it has nowhere to go because there are no rivers carrying water farther downstream. That means the arsenic, and other elements and compounds, can concentrate to unusally high levels. Arsenic is present in Mono Lake at a concentration 700 times greater than what the EPA considers safe.

Wolfe-Simon was invited to use the Menlo Park, Calif., lab of the U.S. Geological Survey and was aided in her work by senior research scientist Ron Oremland, who has studied arsenic in Mono Lake for decades.

The bugs she worked with, an otherwise common bacteria in the halomonadaceae family, thrived without phosphates and with lots of arsenic. She then used cutting-edge instruments to determine that the arsenic was embedded in the core genetic and energy-transfer systems of the bacteria - that it appeared to have replaced (or preceded) the phosphorus.

As she explained, replacing phosphorus with arsenic may seem suicidal, but the two are very similar in their makeup. Arsenic is considered toxic because most living things take it in and treat it like phosphorus, only to be destroyed by the small differences.

She said that while small amounts of the phosphorus remained in the arsenic-based bugs, she was able to determine that it was definitely not enough to supply the presumed phosphorus needs of the cell. That, she said, was being done with the arsenic.

"Sometimes I'm asked why something like this has never been found before, and the answer is that nobody has run the experiment before," Wolfe-Simon said. "There was nothing really complicated about it - I asked a simple question that was testable and got an answer."

Wolfe-Simon said she hopes to test her findings in northern Argentina, where there's an arsenic-heavy ecosystem that also seems to support microbial life.

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