AbstractAbstract

The history of the life–Earth system can be divided into five ‘energetic’ epochs, each featuring the evolution of life forms that can exploit a new source of energy. These sources are: geochemical energy, sunlight, oxygen, flesh and fire. The first two were present at the start, but oxygen, flesh and fire are all consequences of evolutionary events. Since no category of energy source has disappeared, this has, over time, resulted in an expanding realm of the sources of energy available to living organisms and a concomitant increase in the diversity and complexity of ecosystems. These energy expansions have also mediated the transformation of key aspects of the planetary environment, which have in turn mediated the future course of evolutionary change. Using energy as a lens thus illuminates patterns in the entwined histories of life and Earth, and may also provide a framework for considering the potential trajectories of life–planet systems elsewhere.

Free energy is a universal requirement for life. It drives mechanical motion and chemical reactions—which in biology can change a cell or an organism1,2. Over the course of Earth history, the harnessing of free energy by organisms has had a dramatic impact on the planetary environment3,​4,​5,​6,​7. Yet the variety of free-energy sources available to living organisms has expanded over time. These expansions are consequences of events in the evolution of life, and they have mediated the transformation of the planet from an anoxic world that could support only microbial life, to one that boasts the rich geology and diversity of life present today. Here, I review these energy expansions, discuss how they map onto the biological and geological development of Earth, and consider what this could mean for the trajectories of life–planet systems elsewhere.

In the beginningIn the beginning

From the time Earth formed, around 4.56 billion years ago (Ga), two sources of energy were potentially available to living organisms: geochemical energy and sunlight. Sunlight is a consequence of the planet's position in the Solar System, whereas geochemical energy is an intrinsic property of the Earth. Geochemical energy arises when water reacts with basalts and other rocks8,​9,​10. These water–rock reactions—which continue today11—generate reduced compounds such as hydrogen, hydrogen sulfide, and methane8,​9,​10. Oxidation of these compounds releases energy, which organisms can capture and store in the form of chemical bonds. Although sources of geochemical energy can be at or near Earth's surface, they need not be: many are deep within the planet, out of reach of sunlight.

Assuming that life did not parachute in, fully formed, from elsewhere, a number of authors12,​13,​14,​15 have argued that the transition from non-life to life took place in the context of geochemical energy, with the ability to harness sunlight evolving later (Fig. 1). Consistent with this, both phylogenetic16 and biochemical13,17 evidence suggest that the earliest life forms were chemoautotrophs, perhaps living by reacting hydrogen with carbon dioxide and giving off acetate, methane and water13,16. Mounting evidence18,​19,​20,​21,​22 suggests that the transition from non-life to life may have taken place before 3.7 Ga—a time from which few rocks remain23.

Figure 1: Key events during the energy expansions of evolution.
Figure 1

(i) Life emerges; epoch of geochemistry begins. (ii) Anoxygenic photosynthesis: start of energy epoch 2, sunlight. (iii) Emergence of cyanobacteria. (iv) Great Oxidation Event: energy epoch 3, oxygen. (v) Probable eukaryotic fossils appear. (vi) Fossils of red algae appear. (vii) Start of energy epoch 4, flesh. (viii) Vascular plants colonize land; fire appears on Earth. Finally, the burning logs indicate the start of energy epoch 5, fire. The dates of (i)–(iii) are highly uncertain. For (i) I have taken the earliest date for which there is evidence consistent with life20. For (ii) I have taken the earliest date for which there is evidence consistent with photosynthesis18,19,21. For (iii), I have marked the date currently supported by fossil evidence for the presence of cyanobacteria (see main text, ‘Cyanobacteria and the oxygenation of the air’). Tick marks represent intervals of 25 million years. Figure drawn by F. Zsolnai.

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