California Meetings An artist’s rendering of what the Archean earth looked like at the time of the rise of oxygen. The Birth of Oxygen John Abelson This presentation was given at a meeting of the American Academy, held at the University of California, San Diego, on November 17, 2006. John Abelson is George Beadle Professor of Biology, Emeritus, at the California Institute of Technology, Adjunct Professor of Biochemistry at the University of California, San Francisco, and the President of the Agouron Institute. He has been a Fellow of the American Academy since 1985. We take it for granted that our atmosphere thesis was, after the origin of life itself, the The closely linked evolution of photosyn- contains oxygen, but we and most other ani- most important development in the history thesis and the evolution of the atmosphere is mals would die within minutes if the oxygen of our planet. About twelve times as much perhaps the best example of the interdepen- was removed. It is not widely appreciated energy is derived from the aerobic metabo- dence of biological and geological processes. that for half of the earth’s history there was lism of a molecule of glucose as the energy In chronicling the rise of oxygen, I will ½rst virtually no oxygen in the atmosphere. Oxy- obtained from anaerobic metabolism. With- describe photosynthesis and its origins. Then gen appeared 2.45 billion years ago, and it has out the invention of oxygenic photosynthe- I will turn to a discussion of the state of the been present ever since–though not always sis, multicellular organisms could not have earth and its atmosphere before and during at its present level of 21 percent. evolved. Furthermore, the presence of oxy- the rise of oxygen. After the rise of oxygen, gen in the atmosphere leads to an ozone lay- the atmosphere and the oceans went through Photosynthesis produces more than 99 per- er that protects life from the lethal effects of some initially cataclysmic and then very slow cent of the oxygen in the atmosphere. Argu- ionizing radiation. changes. Finally, 540 million years ago–al- ably, the biological invention of photosyn- 28 Bulletin of the American Academy Spring 2007 most 2 billion years after the initial rise of obacterium. In discussing photosynthesis oxygen–roughly the present levels of oxygen and its origin, therefore, it is appropriate to in the atmosphere and in the ocean were at- focus on cyanobacteria. tained. It was only then that multicellular The photosynthetic machinery in cyanobac- life began to flourish. terium is located in a system of layered thyla- The story of oxygen and its effects takes place koid membranes. The membranes enclose an over a long period of time (see Figure 1). interior space, the lumen. The machinery con- sists of pigmented proteins, many of them ex- One way to comprehend this vast expanse of tending across the thylakoid membrane to time is to compare it to the time it took the the exterior space, the stroma. Some of the continents to rearrange themselves complete- Figure 1 proteins and pigments in the thylakoid mem- ly via plate tectonics. Two hundred and twen- brane serve as antennae to funnel light ener- ty-½ve million years ago, all of the continents In oxygenic photosynthesis, the electrons gy into the reaction center. were together in the supercontinent Pangaea. from water are extracted and used to gener- Over 225 million years the continents sepa- ate energy and to reduce carbon dioxide to a The reaction center consists of two complex rated and the Atlantic and Indian oceans were carbohydrate according to the equation: multiprotein assemblies, termed Photosys- formed. This process represents about 5 per- tem I and Photosystem II (psi and psii). At cent of the earth’s history and about one- H2O + CO2 (CH2O) + O2 the heart of both psi and psii is a cofactor tenth of the time period we chronicle here. Since the work of Martin Kamen and Samuel chlorophyll molecule. It is also useful to consider how much biolo- Ruben more than ½fty years ago, we know Figure 2 depicts the major multiprotein com- gical change can take place in 2 billion years. the O2 generated in photosynthesis is entire- plexes involved in photosynthesis. ly derived from H2O. Water is therefore dis- A heritable and selectable change–a muta- We don’t have suf½cient space here to discuss tion–can take place at every cellular division. sociated in photosynthesis according to the 24 equation: photosynthesis in depth, so I will focus on the The earth’s oceans contain about 4 x 10 ml mechanisms of oxygen synthesis. This reac- of water. If we conservatively assume a steady + - 2H2O 4H + 4e + O2 tion takes place in psii. The active site for di- state of 1000 cells/ml in the ocean and a divi- oxygen synthesis, called the Oxygen Evolv- It takes an enormous amount of energy to sion time of one week (during this period ing Center (oec), contains four manganese extract an electron from water because oxy- most cells are unicellular microorganisms), atoms and one calcium atom, coordinated 39 gen has a high af½nity for electrons. One then in 2 billion years something like 10 mainly to one core psii protein. The water- photon of light is required to extract each divisions could take place. Speci½c mutations splitting mechanism is unique; so far, at least, electron, making photosynthesis a four-elec- in bacteria take place at a frequency of about a related metallo-protein has not been iden- -8 tron process. 10 . Even more rapid changes can occur when ti½ed. The oec allows for the integration of genes are transferred between different or- Oxygenic photosynthesis takes place in one a one-electron process (the excitation of cy- ganisms. In 2 billion years there is enormous class of bacteria, namely, cyanobacteria. It tochrome P680) with a four-electron process potential for evolutionary change. also takes place in a number of eukaryotic (the splitting of H2O to form O2). A beauti- organisms, e.g., algae and plants. Photosyn- ful experiment done ½fty years ago by Pierre Photosynthesis thesis is nearly identical in eukaryotes and Joliot and Bessel Kok proved that the oec In photosynthesis, the energy of light is used cyanobacteria because photosynthetic eu- abstracts protons and electrons from water to extract electrons and protons from a karyotes came from a symbiotic event in stepwise to evolve oxygen. Alternative mod- which a primitive eukaryote captured a cyan- els ruled out by this experiment include the donor molecule H2A, which are then used to reduce carbon dioxide: cooperation of four reaction centers to cleave a single mo- + - 2H2A 4H + 4 e + 2A lecule of H2O, and the accu- mulation by one center of CO + 4H+ + 4e- (CH O) + H O 2 2 2 four oxidizing equivalents The donor molecule H2A can be a variety of prior to oxidizing water in a ++ reduced compounds, including H2S, Fe , single concerted step. H various organic compounds, and H O. 2, 2 The oec can now be under- The use of the former group of donors prob- stood more clearly because ably predated the use of water in photosyn- J. Barber in London obtained thesis. The cellular machinery for oxygenic a 3.5A crystal structure of photosynthesis (in which water is used as psii, and K. Sauer, W. Saen- the donor) is, in part, derived from its prede- Figure 2. From Robert E. Blankenship, Molecular Mechanisms of Photosynthesis ger, and colleagues found a cessors. Reprinted with permission from Blackwell Publishing. Bulletin of the American Academy Spring 2007 29 California Meetings oxygen. It seems very unlikely that all of these The closely linked evolution steps used some other oxidant and different enzymes prior to the advent of oxygen and of photosynthesis and the then were somehow altered with the arrival of oxygen. Thus one could make the argument evolution of the atmosphere that the presence of stearanes in the Australian black shales indicates the presence of molec- is perhaps the best example ular oxygen in the ocean 2.7 billion years ago. of the interdependence of Figure 3. From Junko Yano et al., “Where Water is But even though the rocks from which these Science Oxidized to Dioxygen,” 314 (November 3, samples were extracted are correctly dated, biological and geological 2006): 821–825. Reprinted with permission from AAAS. it is more dif½cult to be sure that the biomark- processes. ers were deposited in the rocks at that date. They could have been the result of ground- oec during the Archean eon and that the temper- higher resolution structure of the man- water penetration from the surface or pene- ature was likely warmer than it is now. ganese-oxide core by X-ray absorption spec- tration of oils from younger rocks into the troscopy on single crystals of psii. older rocks. Or they could have been contam- Certainly carbon dioxide would have provid- In photosynthesis the manganese-oxide clus- inated by drilling fluid. Great precautions ed a greenhouse effect, but without oxygen are now taken to avoid this type of contami- in the atmosphere, methane, likely produced ter binds two molecules of H2O. The energy of one quanta of light abstracts one proton nation. Cores are obtained using only water by methanogenic bacteria, could have accu- and one electron. This structure then inte- as the drilling fluid. The exterior surface of mulated to 1000 ppm (it is present at about 2 grates four electron-transfer reactions that the drill cores is shaved off, and the sample is ppm now). The composition of the Archean result in the synthesis of one molecule of taken from the interior of the core.