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Written in Stone

Professor Dianne Newman, PhD ‘98, studies rocks for clues about the origins of photosynthesis–and how chronic infections take hold.

In her office in Building 68, Dianne Newman keeps a polished, spherical rock striped with bands of iron. Found on every continent, such rocks are the most common source of iron ore. And to Newman, specimens like this 2.4-­billion-year-old example yield insights that could help unravel a very knotty part of Earth’s history. When did ancient microbes start producing the oxygen we breathe, and what kind of microbes were they?

Newman didn’t plan to spend her career exploring such questions. She came to MIT in 1993 to get a master’s degree in engineering, thinking she’d work in the field for a few years before going to law school to become a patent attorney. But a class in environmental microbiology left her fascinated by the diversity of bacteria’s metabolisms–the chemical reactions they perform to live. “I learned that bacteria could eat toxic compounds and transform them into benign ones,” she recalls. A project that induced bacteria to convert arsenic into a semiconducting material got her interested in how bacteria might have shaped Earth’s chemical makeup, and she moved to the geosciences department, where she earned her PhD. After seven years at Caltech, she joined the MIT faculty in 2007 as a professor of biology and geobiology.

“Microbes are the best chemists on the planet,” marvels ­Newman. Good enough, in fact, to have reshaped its environment. When our solar system formed 4.5 billion years ago, Earth’s atmosphere was almost devoid of oxygen. The first single-celled life forms, which arose about 3.8 billion years ago, probably lived in the seas and had metabolisms that neither required oxygen nor produced it as a by-product. Some of them subsisted on iron; their metabolic processes changed the iron’s chemical state and created the deposits in Newman’s rock. Others probably fed on sulfur.

And then something happened that would make possible animal and plant life as we know it. Some bacteria began using sunlight to split water into hydrogen, which they used to make fuel, and oxygen, which they released as waste. Thanks to oxygenic photosynthesis, the atmosphere and the shallowest ocean water had significant levels of oxygen by about 2.4 billion years ago; by about 540 million years ago, oxygen levels were comparable to those seen today.

The question of which organism first began producing oxygen, and when, is one of the great mysteries in Earth’s history. “It’s a really hard problem but really seductive,” says Newman.

To answer it, Newman and others at MIT and around the world focus on rocks like the one in her office. Just like dinosaur bones, the remains of bacteria living in the ancient seas were incorporated into rock over millions (in the bacteria’s case, billions) of years. Researchers know that certain compounds are made only through processes carried out in living organisms, so when they see such compounds in a rock, it means that the rock reflects traces of ancient life. Geobiologists interpret these bacterial fossils by comparing the chemical compounds in them with those created by modern bacteria that still rely on ancient metabolic processes. Through such analysis, they hope to pin down which microbes made the chemical compounds left in the rocks. “You have to look at the function of these chemicals in lots of living organisms,” says Newman. “This kind of logic links us to the past.”

One of the most important chemical traces left by ancient bacteria is a group of compounds called 2-methyl-BHPs. In 1999, Roger Summons, an MIT professor of geobiology, and colleagues found these compounds in 2.5-billion-year-old rocks from the ­Hamersley Basin in western Australia. These rocks, from an iron mine, are similar to the polished one in Newman’s office. Today, oxygen-producing photosynthesizers called cyanobacteria are the primary producers of these BHPs. For this reason and many others, including certain characteristics of the Hamersley site, Summons and others have interpreted the find as evidence that cyanobacteria were carrying out modern photosynthesis 2.5 billion years ago. “The logic was that these compounds are made by cyanobacteria; cyanobacteria do oxygenic photosynthesis; therefore oxygenic photosynthesis was going on at that time,” says Newman.

Newman thinks that her own research casts doubt on this conclusion. She has been studying another strain of bacteria that produce BHPs: so-called purple bacteria, which cannot use water to produce oxygen. Instead, they oxidize iron, hydrogen, or various organic compounds. “We’re trying to figure out the function of [BHPs] in the cells that make them today,” she says. “Our preliminary findings indicate that BHPs have no direct connection with photosynthesis.” ­Summons, who collaborates with Newman on some of her research, doesn’t take her skepticism personally; he’s confident that her work will lead to important insights into these compounds and, especially, why and how bacteria make them. However, he also points out that her findings don’t disprove the theory that chemical traces left by cyanobacteria are preserved at Hamersley.

Meanwhile, Newman’s work with bacterial compounds known as phenazines is illuminating a problem more immediate than the mystery of how our oxygen-rich air came to be. By changing the way scientists understand these organic molecules, her research could lead to new treatments for chronic bacterial infections.

Phenazines have long been classified as “secondary metabolites,” by-products of the processes that produce more critical metabolic compounds. They’ve also long been known to act as antibiotics. But Newman has demonstrated that phenazines also have profound effects on microbial survival and development.

Newman got the idea for this research while studying bacteria that, strange as it sounds, use iron-containing rocks to “breathe.” Humans use oxygen to burn the carbon in, say, a tuna sandwich, creating energy; the oxygen’s role is to accept electrons from the carbon. Iron plays a similar role for the rock-breathing bacteria, which get their energy when they transfer the electrons in carbon-containing compounds like glucose to the iron in rocks. It’s not breathing in the human sense–the iron itself does not enter the cells, as oxygen enters our lungs. Rather, rock-breathing bacteria pass an electrical current to the iron using molecules that act as electron shuttles. These molecules transport electrons from one bacterial cell to the next and ultimately to the surface of a ferrous rock, like the hands of an audience ferrying a crowd-surfing rock star. Newman and her colleagues hypothesize that phenazines might act as electron shuttles in other bacteria.

If they’re right, their insight could have broader implications, because it addresses what Newman calls “a generic problem bacteria face growing on any surface.” Few bacteria dwell on their own. No matter where and how they get their energy–whether they savor the sugars in the crevices of your teeth or slurp sulfur from undersea vents–most bacteria live in thick, clingy communities called biofilms. Inside a biofilm, some of them will be closer than others to the chemicals they need to conduct their energy-producing reactions. As Newman thought about the way iron-breathing bacteria use electron shuttles to transport their electrons from deep within a biofilm to a rock surface, she realized that bacteria growing in biofilms in our bodies might do something similar.

Newman decided to test the importance of phenazines produced by the human pathogen Pseudomonas aeruginosa, which causes serious chronic infections in people who have cystic fibrosis or whose immune systems have been compromised. Living in the lungs, these bacteria would run into the same problem as the rock breathers worlds away: those in the middle of the biofilm would be isolated from an important energy substrate, in this case oxygen.

To test whether these bacteria could use phenazines to overcome the challenges of communal living, researchers in Newman’s lab engineered two mutant strains of them. One strain couldn’t make phenazines, while the other made them in great quantities. When ­Newman and her collaborators grew the bacteria in petri dishes, they saw differences in the architecture of their communities. The overproducing strain grew in a tight, smooth layer, spread out like Los Angeles. The phenazine-free strain also spread out over a large area but grew in high towers, built up like New York City–presumably to maximize each cell’s exposure to the oxygen in the air.

These results are promising; now Newman must perform tests to see how the two mutant strains grow in the lung. If Pseudomonas needs phenazines to survive, researchers could, in theory, develop therapies that prevent the bacteria from synthesizing or making use of them; that could help eradicate chronic infections.

“Accessing oxygen today is just as much a problem as accessing a mineral was in the past,” Newman says. It’s just such connections that make geobiology a rich and surprising vein of knowledge, not just about the planet’s history but about our present.

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