Breathing easy at night: Atmospheric oxygen and biological evolution
Van Leeuwenhoek Lecture on BioScience.
Don Canfield (B.S. in chemistry, Miami Un. 1979, M.Phil. 1984 and PhD in geochemistry, Yale Un., 1988) had positions at Yale University, the University of Michigan, NASA-Ames, Arhus, Georgia Institute of Technology, Max Planck Institute for Marine Microbiology in Bremen, and Odense University, where he is professor of ecology (1996 until present). He has been co-director of the Danish Center for earth System Science (1997-2005) and is director of the Nordic Centre for Earth Evolution from 2005 on.
The work of his group is multidisciplinary and involves elements of microbial ecology, biogeochemistry, and geology. He and his coworkers are interested in understanding the cycling of bioactive elements of the modern earth, and into the distant geological past. They are particularly interested in understanding how the chemistry of the earth surface has changed through geologic time, and how this changing chemistry might have influenced the nature and structure of ecosystems and the evolution of life. This work takes them to the modern environments including marine sediments, anoxic marine basins, and anoxic lakes as well as to rocks deposited long ago. In total, his group aims to understand how to read the chemical traces preserved in ancient rocks and how these traces can tell of the nature of ocean and atmospheric chemistry.
His group also explores modern microbes to understand how environmental variables like temperature, oxygen content, trace metal availability, or sulfate levels might influence their activity as well as the nature of any metabolic products they might leave behind. In this regard, they have been particularly interested in exploring the factors influencing isotopc fractionation associated with sulfur metabolism. Through this work they have been able to piece together the history of seawater sulfate concentrations and the relationship between sulfate levels and concentrations of atmospheric oxygen.
More than any other element, oxygen shapes the current biosphere. It is produced by photosynthesis and is used to respire most of the organic matter at the Earth surface. However, this is not always been the case. During the first 2 billion years of Earth history, oxygen concentrations were likely > 100.000 times less than present levels. Could an anaerobic atmosphere have existed with so little oxygen? This question is addressed through growth experiments conducted on E. coli utilizing special oxygen sensors with ultra-low oxygen-detection limits. We find that E. coli can grow and respire oxygen at oxygen concentrations < 2nM which is 100.000 times less than found today in air-saturated water. After about 2,4 billion years ago, oxygen concentrations rose to levels that are uncertain. There is a prevailing view, however, that these levels were insufficient to allow respiration by aimals thus preventing their evolution. The minimum levels of oxygen required for animals (as a group), however, is poorly known. We attempt to define levels required for animal respiration through a variety of respiration and behavior experiments on two different marine sponges. We show that sponges feed and respire at oxygen concentrations ranging between 1 and 4% of present levels. This, therefore, might be viewed as a possible minimum oxygen requirement by early animals. Atmospheric oxygen may have attained these levels well before animals, implying that other factors controlled the timing of animal evolution.