A theory that suggests the oceans were far poorer in oxygen 1 billion to 2 billion years ago may answer an important evolutionary puzzle, says a pair of researchers from the University of Rochester and Harvard University in today's issue of Science.

For some unknown reason, eukaryotes, the kind of cells that make up all organisms except bacteria, got off to a slow start compared to their prolific bacterial cousins until about 2 billion years after they first appeared in the geologic record. The Rochester and Harvard scientists propose that a new and controversial model of the Earth's oceans may be able to account for the billion-year mystery.

Ariel Anbar, associate professor of earth and environmental sciences and chemistry at the University of Rochester, and Andrew Knoll, professor of evolutionary and organismic biology at Harvard University, suggest that although scientists have long thought that the oceans' history had only two major stages, a third, intermediate stage could explain certain fossil patterns better than the two-stage model could.

The two traditional stages-anoxic (without oxygen) in the earliest years of Earth's history, and the oxic oceans of today-were defined by the disappearance of banded iron formations, massive layers of iron that exist in the rock strata around the world, about 2 billion years ago. To form these deposits, the oceans must have had high concentrations of dissolved iron. But since iron is removed from water when it reacts with oxygen, these bands of iron could only form in an anoxic ocean. This suggested that the oceans became oxic about 2 billion years ago. However, an intermediate ocean stage recently proposed by D. E. Canfield of Odense University, Denmark, suggests that the deep sea did not become rich in oxygen, but rather rich in hydrogen sulfide-the compound that gives rotten eggs their foul smell-between 2 billion and 1 billion years ago. According to Canfield, the oceans did not turn oxic until after 1 billion years ago. The model can also explain the end of banded iron formation because iron is also removed from water when it reacts with hydrogen sulfide.

After learning about Canfield's hypothesis, Anbar and Knoll began to consider its biological consequences. They realized that if the Canfield ocean model were correct, then some metals other than iron would have reacted with the sulfidic water and become very scarce. Some of these metals are important to life in general and to eukaryotes in particular. One of these metals, molybdenum (Mo), is needed by eukaryotes to help take in nitrogen from seawater. If molybdenum were in short supply, eukaryotes would have had a tough time getting enough nitrogen to survive. Today molybdenum is more abundant in the oceans than any other metal because it coexists well with oxic water. So after 1 billion years ago, when Canfield suggests the oceans became thoroughly oxygenated as they are today, molybdenum would have become abundant enough allow eukaryotes to take in the much-needed nitrogen and flourish.

This scenario, Anbar and Knoll found, fits the evolutionary evidence. Fossils and the presence of biological compounds suggest that eukaryotes arrived on the scene as far back as 2.7 billion years ago, but were not as successful at proliferating as bacteria until after 1 billion years ago.

"The ancient biological record is very hard to read," says Anbar, "but it looks as though something changed at that time. We know that metals are an important link between ocean chemistry and biology today, so it makes sense that a similar link operated in the distant past."

Anbar acknowledges that more data is needed to determine if Canfield's model is correct, but hopes that the possible connection between the ocean chemistry of Earth's "middle age" and the record of eukaryotic evolution will spur more research into the complex history of the oceans and their effect on the evolution of life.

"It's remarkable that we aren't sure if the oceans were full of oxygen or hydrogen sulfide at that time," says Anbar. "This is a really basic chemical question that you'd think would be easy to answer. It shows just how hard it is to tease information from the rock record and how much more there is for us to learn about our origins." Anbar and Knoll are actively working on new measurements to tackle the problem.

The research was funded by the National Science Foundation and the NASA Astrobiology Institute.