Profile of Donald E. Canfield

An ecologist might say that the answer to nearly every question about the origin and evolution of life on Earth can be found in the ocean, where reactions fueled by ancient microbes have changed our planet's chemistry over the eons. Donald Canfield, Professor of Ecology and Director of the Nordic Center for Earth Evolution at the University of South Denmark, has spent his career studying oceans and lakes to understand the progressive oxygenation of the atmosphere through time, ultimately permitting the development of large motile animals.

Donald E. Canfield.

Canfield, 53, was elected to the National Academy of Sciences in 2007. His Inaugural Article, published in PNAS in November 2010, demonstrates that Escherichia coli, a well-known lover of oxygen, or “aerobe,” can grow in oxygen concentrations 100,000 times less than those found in regular air, suggesting that aerobic organisms evolved much earlier than believed (1).

A native of Cincinnati, OH, Canfield spent his childhood in a handful of other midwestern cities where his father, an engineer, was transferred. Canfield was an inquisitive child with a strong interest in how things worked. “I was famous for asking question after question, and not every adult was so patient. But my dad, he just answered them all,” Canfield remembers. “Whenever he was working on something, he always let me come and see what was going on, and I would ask more questions. I never would have developed my interest in science if my father wasn't extremely patient.” Canfield also credits his grandfather for cultivating his fascination with the ocean. “My grandfather was always crazy about the water, and I was his fishing buddy,” Canfield recalls. “He had a little cottage in the Florida Keys, and my family would go there frequently. By the time I was 13 or 14 years old, I decided I wanted to do something with the oceans if I could.”

Rock, Water, and Ice

Canfield enrolled in college at Miami University in Oxford, OH, as a chemistry major. He enjoyed his studies, but it was not until he discovered aqueous and natural chemistry with his first mentor, Bill Green, that he really got excited about science. “That changed my whole life,” Canfield recalls. “All of a sudden, chemistry became extremely exciting when I could see it being applied to the natural world.” His first taste of scientific research came at Acton Lake, about 10 miles from Miami University. The idea was to determine how calcium was removed from the lake by measuring calcium carbonate saturation in the water. “I was just in heaven,” he says. “I thought that was the most exciting thing you could do, to go out and try to sort out something in the natural world.” (2)

During Canfield's senior year of college in 1979, he recalls, “Green was writing this grant to go to the Antarctic to work on some dry valley lakes. I finally screwed up the courage to ask him if I could maybe go along, and he said, ‘Yes, absolutely, that would be fantastic.’” Of the voyage to Antarctica at the age of 22, Canfield says, “I was there for 3 months, and it seemed as if time stood still. All the experiences were so new and so magnificent. The best thing was going out and spending time in the field, out in dry valleys where you didn't see anything familiar. There was no grass or birds or trees or living thing you would recognize from home. It was just rock, water, and ice. It was fantastic.” (3)

By then, Canfield was certain he wanted to pursue a doctoral degree, and he enrolled in the geology department at Yale University with Bob Berner as his supervisor and mentor. “Through Bob's influence, I became really interested in how microbes influenced the chemistry of the oceans,” Canfield says. Marine sediments were a good place to start because of the high concentrations of microbial communities and chemical reactions (4). His dissertation focused on the interplay between the sulfur and iron cycles in marine sediments and the role of these cycles in oxidizing organic matter. He found that iron oxides, which were abundant in sediments, were the primary determinant of sulfide concentrations. Canfield's dissertation further revealed that iron reduction and sulfate reduction by microbes were important contributors to organic carbon mineralization (5). Along the way, Berner piqued Canfield's interest in the evolution of ocean and atmospheric chemistry. “That grabbed me too; the idea that these processes we study today actually change or were different in the geological past,” Canfield says. “Not only that, but maybe there were some tools we could develop to better understand how microbial processes had evolved through geological time and how they interfaced with the evolution of atmospheric and ocean chemistry. This opened up a whole horizon of possibilities for me.”

Exploring the Elements

After receiving his PhD in 1988, Canfield studied early Earth evolution and microbial ecology with Dave Des Marais at the National Aeronautics and Space Administration's Ames Research Center in California. “That was about the best move I possibly could have made. This introduced me to studies of deep Earth history as well as modern microbial ecology,” he says. The research took Canfield to Guerrero Nogro, in Baja California, Mexico, to study the oxygen and carbon dynamics of modern microbial mats (6).

“While working with Dave, I was lucky enough to meet Bo Barker Jørgensen,” Canfield says. “Bo was a scientist I had admired all along, and he was one of the people doing the kind of microbial ecology mixed with biogeochemistry that I really understood and related to. He invited me to come and do some work in Århus, Denmark, his home base.” Since then, Canfield's career has meshed Earth history, microbial ecology, and geochemistry as well as the cycles of elements like iron, sulfur, chromium, carbon, and oxygen.

In Århus, Canfield met his future wife, Marianne prip Olsen, who was then a biologist and is now a writer. After a few years in Bremen, Germany, where Jørgensen and Canfield worked at the Max Planck Institute, Olsen and Canfield returned to Denmark and Canfield joined the University of South Denmark. There, he helped to found the Danish Center for Earth System Science and now directs the Nordic Center for Earth Evolution, a collaboration among 35 researchers in Odense, Copenhagen and Stockholm, Sweden. Canfield's work at the center has earned him an ever-increasing reputation in his field: He is a foreign member of the Royal Danish Academy of Sciences and Letters and a Fellow of the Geochemical Society and European Association of Geochemists, the American Association for the Advancement of Science, and the American Association of Microbiologists. In 2010, he won the Vladimir Vernadsky Medal from the European Geosciences Union.

These honors, in part, reflect Canfield's discoveries about the consequences of rising atmospheric oxygen levels on the evolution of ocean chemistry. Perhaps the most significant rise in atmospheric oxygen, “The Great Oxidation Event,” began about 2.4 billion years ago, during which time cyanobacteria began releasing oxygen. The blue microbes, known for generating energy through photosynthesis, effectively transitioned the Earth's atmosphere over the course of 2 billion years from nearly no free oxygen to the high levels present today.

Before the Great Oxidation Event, the deep oceans contained abundant amounts of dissolved iron, which contributed to the spectacular banded iron formations commonly found at the time. Most geologists assumed the dissolved iron was permanently removed by oxygen from the Great Oxidation Event, which permeated the deep ocean. Canfield recounts, “The problem was, if we looked at our indicators of ocean chemistry, there were plenty of indications for anoxic iron-rich deep ocean chemistry before the Great Oxidation Event, and after it, the deep iron seemed to largely go away.” Until that point, he says, the traditional explanation had been that oxygen levels rose and the deep ocean became oxygenated, which subsequently reduced iron levels. “I wasn't too comfortable with that idea, because it required more oxygen than most geologists, including myself, were prepared to think was around then,” Canfield says.

Canfield's “Aha!” moment came when he compiled a history of the isotopic composition of sulfur through geological time. It became clear to him that a large increase in sulfate concentrations coincided with the disappearance of banded iron formations, around the same time as the Great Oxidation Event. Putting these observations together, Canfield proposed that the rising oxygen levels enhanced the conversion of sulfide minerals to sulfate on land. Without much oxygen, sulfate would not have effectively weathered from the continents, but the accumulation of oxygen boosted the oxidation of sulfides, which, in turn, allowed more sulfate to enter the oceans. With more sulfate entering the oceans, Canfield says, more sulfate could be converted to sulfide by a microbial process called sulfate reduction, in which sulfide removes iron. The world's oceans likely persisted in a state of elevated sulfide concentrations from about 1.85 to about 0.80 billion years ago, a state now referred to as a “Canfield Ocean.” (7)

“When I first made the proposal, it got a pretty silent reception,” Canfield recalls. “I don't think people knew what to do with it.” After a few years, however, researchers began to show greater interest. Twelve years later, Canfield's theory remains popular, although he and other researchers have gradually modified it as research reveals how the chemical structure of oceans changed over time. “It may not be that the ocean was a big sulfidic pool like I first described it,” Canfield says. “It seems that the sulfide was more concentrated in oxygen minimum zones, like you have in present-day oceans, but there was still a high prevalence of sulfide in the oceans.” (8)

Aerobic Evolution

Canfield is also interested in what life was like early in Earth history, especially for the earliest aerobes. “When we think about aerobes, we think about [humans and] animals and our need for high levels of oxygen,” he says. In the Archean Eon, before the Great Oxidation Event, oxygen was probably 100,000 or more times less abundant than today, but it is not certain what levels were sufficient for aerobic communities to survive and flourish and when these levels first appeared.

To answer that question, Canfield and his colleagues measured the growth of aerobes under limited oxygen conditions using a new sensor developed by one of his collaborators, Niels Peter Revsbech. The finely tuned polarographic sensor uses a large cathode to scrub all oxygen periodically from the tip of the sensor, allowing for the detection of minute concentrations of oxygen. In his Inaugural Article, Canfield and colleagues (1) report that E. coli can grow aerobically at nanomolar oxygen concentrations, which are 100,000 times lower than present atmospheric levels and two to three orders of magnitude beyond what has been measured for other aerobes. In fact, Canfield says that E. coli will continue to grow at even lower levels, well within the picomolar range, beyond the polarographic sensor's detection limits. In fact, Canfield's models suggest that E. coli can grow at oxygen concentrations at which geochemical indicators say the Earth would have been essentially anoxic, he says.

The findings imply that aerobes could have existed and even thrived before the Great Oxidation Event, and possibly before the evolution of cyanobacteria. Canfield's theory rests on two bodies of evidence. First, oxygen-hungry steroids existed before the Great Oxidation Event, when there was supposedly no free oxygen. Second, “oxidase enzymes are really, really ancient; probably more ancient than cyanobacteria,” Canfield says. “So you have this enzyme system, ostensibly used to bind oxygen, which is older than the organisms that produce it.”

In principle, at least, nonbiological processes are capable of generating small amounts of oxygen, Canfield says. Hydrogen peroxide, for example, is produced in the atmosphere, where it splits into hydrogen and local pockets of oxygen that could potentially maintain a community of aerobic bacteria. “This picture points to the possibility that aerobes might have been alive before cyanobacteria, which I think is pretty incredible,” he says.

Aerobic bacteria might have first evolved and lived in small ponds and lakes as well as in the soil, Canfield suggests, because that is where nonbiological sources of oxygen were likely concentrated. “I may be wrong, but I imagine an early community of aerobes on land, because that's where you might have accumulated a bit of peroxide or other nonbiological sources of oxygen,” he says. If, on the other hand, aerobes evolved in concert with cyanobacteria, which most Earth scientists believe occurred well before the Great Oxidation Event, terrestrial environments might still have been an important haven for aerobes. “This is because the very small concentrations of oxygen available in the atmosphere could have flushed the very upper layers of soils or very shallow aquatic environments,” he explains.

Canfield sees oxygen as an essential key to understanding the evolution of life on Earth, particularly how oxygen levels facilitated the transition from pre-Cambrian to Cambrian life forms, when large motile animals first evolved. “This really fascinates me, but there are lots of tricky aspects to the carbon cycle that we have to sort out, because the carbon cycle was working very differently back then,” he says. One aspect in particular, the relationship between early animal evolution and the chemical evolution of the environment, will form the focus of Canfield's future work.

A recent discovery along these lines shows that a burst of oxygenation about 400 million years ago is synchronous with the evolution of vascular plants and large predatory fish. (9) “The evolution of plants drove atmospheric oxygen to higher levels, which then allowed for the evolution of larger predatory animals. I think that's a pretty neat coupling,” he says.

The ancient Earth is not the only thing that Canfield thinks about. Climate change is also on his radar. One issue that worries him is how the nitrogen cycle may adjust itself in response to higher temperatures and carbon dioxide levels this century. He notes, “I hope that with my background, I can have some voice on issues related to global climate change.”