[MUSIC] Welcome to the Origins course at the University of Copenhagen. The history of life on Earth is closely tied to the history of oxygen. Oxygen makes up 21% of the air that we breathe and makes Earth habitable for complex life. Yet Earth was born anoxic and many single organisms actually live in the absence of oxygen. As we shall see, oxygen has played a very special role in the evolution of life and for the history of our planet. My name is Tais Dahl and I'm a scientist at the Natural History Museum of Denmark. In this first lecture on the history of oxygen, I will introduce Earth's long-term oxygen cycle, how oxygen is produced and destroyed, and also why it accumulated in Earth's atmosphere and oceans. Also, I will give you an idea how much oxygen animals require because a rise in atmospheric oxygen has long been thought to trigger the emergence of animals on Earth. In my second lecture, I will describe the history of oxygen over the past 4 billion years and some of the evidence. In the third lecture, I will discuss interactions between the evolution of life and oxygen in the environment. I hope this will inspire you to think more about how the Earth's system functions. I think we are addressing some of the most fundamental questions about the world we live in. Has oxygen in the environment shaped the evolution of life, or is it vice versa, biological evolution that has determined oxygen levels on Earth? Our planet Earth is special because it is habitable for life and because life is flourishing everywhere in Earth's surface environment. Organisms live in deserts and in glaciated regions, in the tropics, at the poles, in the atmosphere, on land, in the oceans and soils, and even inside ice, soils and cracks in rocks. Life is present essentially everywhere in Earth's surface environments, and organisms make a living in many different ways. As far as we know, this stands in sharp contrast to all other planets and moons in our solar system. For a space traveler, the habitability of our planet can be seen many light-years away because of the characteristic composition of Earth's atmosphere. Today, oxygen accounts for 21% of Earth's atmosphere. When I say oxygen, I actually mean molecular oxygen or free oxygen. 99% of all free oxygen is in the atmosphere, and the last 1% is dissolved in the oceans. All of the oxygen is produced by biology. Earth's atmosphere would be anoxic if it wasn't for the constant oxygen production in photosynthetic life. Molecular oxygen is a reactive gas that allows your fuel to burn and your bike to rust. Because oxygen is a gas, we only know about its history on early Earth from indirect measurements. I will outline this history in the second lecture, but before that, I will introduce you to the modern oxygen cycle on Earth and why we think oxygen is central for the understanding of the evolution of life. We have learned that Earth was born anoxic, and that oxygen levels have broadly increased over time. We also know that oxygen is used for respiration in all larger complex life forms, including humans. Humans get energy from burning fuel with oxygen through a process called aerobic respiration. Roughly 20% of the energy we obtain from food goes to power our brains. We know that from experiments that humans become lethargic, dizzy when oxygen levels are below 75% of present day atmospheric level. It appears that healthy brain function requires more than 75% of P-A-L. We also know that far the most oxygen is produced by oxygenic photosynthesis in cyanobacteria, algae, and plants. Without oxygenic photosynthesis, oxygen would have been a trace gas at ppm level concentrations in the atmosphere. Therefore, it is clear that we could not have lived here on Earth until the first cyanobacteria had innovated the biological machinery to produce oxygen. Or rather, humans would not be here until oxygen had accumulated to sufficiently high levels in the environment to make air breathable for us. To appreciate the significance of oxygen for life, you need some basic insight to how oxygen is produced and consumed. You need to understand that many bacteria live in permanently anoxic settings and that oxygen is not a general requirement for life. Nevertheless, those who consume oxygen are powered with more energy than those who don't, and this has affected the evolution of life and how resources are distributed in the biosphere. So today, we will visit my colleague, Michael Kuhl, who is a professor at the marine biology lab here at University of Copenhagen. He's making experiments with cyanobacteria, which were the first organisms to produce atmospheric oxygen. In fact, cyanobacteria were the first to evolve the biological machinery for oxygenic photosynthesis more than 2 and a half billion years ago. This strategy has been tremendously successful on our planet, and today, plants and algae have also adopted this strategy. So here you see a culture of cyanobacteria. Cyanobacteria, they produce oxygen as a result of their photosynthetic metabolism. The reason for their success on Earth is quite obvious. Cyanobacteria use solar power to produce new organic matter from some of the most abundant molecules on Earth, water and carbon dioxide. The biochemistry of oxygenic photosynthesis is actually rather complex. It involves two different photo systems to harvest energy from sunlight, and it also involves the rubisco enzyme. So, rubisco is an enzyme that fixes CO2 gas and converts that to organic biomass. Nevertheless, the resulting reaction is rather simple. Carbon dioxide and water is consumed to produce a building block in organic matter. The waste product of this process is oxygen, which can then accumulate in the atmosphere and surface ocean where photosynthesis occurs. So, oxygenic photosynthesis basically stores solar energy in organic compounds as it builds a long molecule from smaller simpler molecules. So these longer, more complex organic molecules contain chemically bound energy that can then be released again when split back into smaller molecules. This occurs by many anaerobic and aerobic processes. So we are all familiar with aerobic respiration because this is actually the same chemical process that we exploit for living. Basically, by aerobic respiration we extract the chemical energy in the long organic compounds by consuming oxygen and releasing carbon dioxide and water. Here you can see examples of fossil cyanobacteria in the geological record. For example, we know of these cyanobacteria in 2 billion year old cherts from Belcher Island in northern Canada. Eoentophysalis forms irregular colonies of ellipsoidal cells. These fossils are surprisingly similar to modern-looking cyanobacteria. Entophysalis is a well-known mat-dwelling cyanobacteria today, where it grows in hypersaline marine environments. It is found in the intertidal zone globally, for example, off the coast of Abu Dhabi and in Shark Bay in Western Australia. Cyanobacteria also built extensive microbial mats 1.5 billion years ago, as we can see recorded in sediments from northern Siberia. Michael Kuhl has collected modern microbial mats, which nicely illustrates the power of oxygen in the biosphere and how it leads to a chemical hierarchy in nature. Those who respire oxygen live closer to the productive cyanobacteria, whereas anaerobic organisms take over once all the oxygen is used up. So, indeed, here we have a microbial mat, which I sampled in a hypersaline lagoon in France. So, if you take a closer look on these cross sections through these microbial mats from a salty lagoon, you see this piece here is actually about a centimeter deep. And you see again this slimy matrix which connects and embeds all the microbes in the mat. See the top layers here. You have this deep green, over here a little bit orange, layers. This is actually where the cyanobacteria, the actively growing cyanobacteria reside. This kind of mat actually only grows about one to two millimeters per year. Light is attenuated very strongly in this dense matrix so there can only be photosynthesis in the upper few millimeters. But you also see that there are layers, older layers here. You can see there are stratifications. These are remnants of older growth seasons, so to say. So, once a biomass gets buried into permanently anoxic zones, the degradation of biomass goes much slower. And actually, also the cyanobacteria here make a lot of structural components, slime sheets, other compounds, polymers, which are not very easily degradable, and they are left behind in the older layers here. So we can actually look back in time by looking on such a cross section here, looking on the different layers. But let's look at some real data. So, one can actually measure oxygen distributions in microbial mats using specialized equipment like such an oxygen microsensor that can be positioned inside the mat. And the kind of data that you get out of it, you can see here on the screen, shows you actually the oxygen distribution in the mat. So, here we have an oxygen concentration profile measured in the microbial mat in darkness. So we have the oxygen concentration up here, zero oxygen here, and increasing oxygen levels in this direction. And here we have the depths inside the mat. We have the surface of the microbial mat up here, zero. We have one millimeter depths here, two millimeters, three millimeters, and so forth. And we see that oxygen penetrates only about three millimeters in the darkness. So, this was the situation in darkness, when you have no light on the microbial mat. Let's try and look how the chemical conditions in the microbial mat change when we illuminate it with light, and let's try to measure the oxygen. So, we've illuminated the microbial mat now for about half an hour. And we'll try to repeat this experiment and measure the oxygen distribution with depths. So let me start the experiment. So now the microsensor is measuring in different distances from the mat surface. You can actually see the number up here. This is 0.8 or 800 micrometers above the mat. And we can see the oxygen level that the sensor measures up here as the thick, blue line. And so it simply measures the oxygen at every single depth step as it moves closer and closer to the mat. And we already see now that oxygen is actually slowly increasing as we approach the mat, but this increase will become more and more dramatic as we get closer to the mat surface. As we see here, indeed, oxygen changed quite significantly. We already now are reaching levels at the surface of the mat, almost 200% of the oxygen level in the water above here. So very high oxygen production due to the very high density of cyanobacteria that produce the oxygen. The high density of the cyanobacteria also cause a very dense matrix that absorbs light. So light attenuates very efficiently. And in such mats, you typically only have photosynthesis in the uppermost millimeter, maybe two. And you see now that we already below the peak. So, photosynthesis peaked about half a millimeter below the mat surface. And now oxygen starts to to decrease in concentration again. And this is because now photosynthesis becomes increasingly light-limited. And at the same time, of course, there's oxygen being respired by the eukaryotes and the prokaryotes present here. In principle, protists, other eukaryotes, as well as prokaryotes, bacteria, archaea are participating in this process. And we see that zones of the mat, which were in darkness only subject to moderate oxygen levels, actually are now exposed to very high oxygen levels, higher than the aerated water above the mat. We can also see that oxygen will not reach zero at three millimeters depths as it did in darkness. It will actually penetrate significantly deeper in this case. So, oxygenic photosynthesis up here pushes down oxygen, more oxygen, deeper into the mat. And that, of course, also affects the microbial processes there. So, first of all, there can be aerobic respiration in a deeper zone of the mat. But also the presence of oxygen will affect the anaerobic processes. Some of the anaerobic processes are inhibited by oxygen, cannot take place, or can only take place in deeper layers. So, some of these anoxic processes are pushed deeper down into the mat during daylight. And as daylight then goes away again, during night, these anoxic processes can again occur closer to the microbial mat surface. And this is a daily recurring change because changes in light will immediately affect the oxygen production, and thereby, the oxygen concentration distribution, and thereby, the whole zonation of the oxic and the anoxic processes in the microbial mat. So, the sensor is now approaching five millimeters and you see that we are approaching zero oxygen, which is this line. So oxygen has been pushed deeper down. Before motile animals evolved, microbial mats were quite common in shallow areas of the ocean. Here's an example of a fossilized microbial mat. This is what we call a stromatolite. We see these layered structures, wavy lamina, situated in successions of marine sediments. Stromatolites were actually quite common in the Precambrian, but rather scarce in Phanerozoic sediments. This change from a microbial world to a world with animals took place in the Neoproterozoic. In northeastern Greenland, this is beautifully exposed in the rock's stratigraphy. We can simply walk from older strata lower in the section with stromatolites and then up section and find the first real body fossils of animals. We find the first, these small shelly fossils, and then later these trilobites. It has long been argued that the emergence of animals was made possible by a rise of atmospheric or oceanic oxygen levels some 600 million years ago. But the first metazoa were sponges and they evolved in the Neoproterozoic, perhaps even before the Sturtian glaciation more than 700 million years ago. Experiments with modern sponges show that they survive and grow at oxygen levels of only 1% of present day level. This is much too low for human brain function. Humans and many animals would have suffocated under such conditions. At present, we think there was enough oxygen in the surface ocean for sponges to breath already 1 billion years prior to their emergence. Therefore, the late appearance of sponges is not just explained by the ability or inability to survive. It could well be that oxygen levels had to be higher than this simply to ensure a more stable habitat. Before we discuss potential links between the origin of animals and oxygen availability, you need to understand what it takes to change oxygen levels on Earth. The global production of oxygen by oxygenic photosynthesis is closely matched by the rate of oxygen removal when organic compounds are aerobically respired. If respiration did not balance out the photosynthetic production, then the oxygen content of the atmosphere would, in fact, double in only 6,000 years. However, half a percent of the organic matter produced is buried in ocean sediments. This means that this carbon is not decaying with the help of oxygen. As a result, some oxygen is left behind elsewhere in the atmosphere and oceans. Half a percent may not sound like much, but every mole of organic carbon buried in sediments leaves one mole of oxygen behind in Earth's surface environments. Organic carbon burial is the principal source of oxygen to the atmosphere and oceans. Popular speaking, we say that oxygen is leaking from the carbon cycle. There's also oxygen leaking from the global sulfur cycle when pyrite sulfur is buried in sediments. The oxygen leaking from the sulfur cycle works more or less the same way as for carbon. And to keep things simple, I will not address the sulfur cycle further here. Now, oxygen is a powerful oxidant and the leftover oxygen produced by organic carbon burial can be destroyed by several other abiotic processes. First of all, oxygen is destroyed by reaction with reducing gasses of methane and hydrogen coming from volcanic and metamorphic outgassing from the Earth's mantle and crust. Secondly, oxygen is removed during oxidative weathering, where oxygen reacts with reduced mineral phases and organic compounds in crustal rocks. Third, oxygen reacts with the salt, iron and manganese cations in the anoxic parts of the ocean. And lastly, hydrogen escape to space is a source of oxygen. This source of oxygen was mainly significant in the Archean, when hydrogen gas was more common in the atmosphere. The reducing sinks for oxygen were greater in the Archean and Proterozoic oceans than they are today, and that would have kept the oceans anoxic and the atmosphere with very low oxygen levels. So, to sum up, overall the history of oxygen is closely tied to the history of organic carbon burial and pyrite sulfur burial. Geochemists can assess how much organic carbon is actually buried over the history of Earth and thus how much oxygen was leaking to the atmosphere at any point in geological history. [MUSIC]
