Electrons, life and the evolution of Earth's oxygen cycle

Abstract

The biogeochemical cycles of H, C, N, O and S are coupled via biologically catalysed electron transfer (redox) reactions. The metabolic processes responsible for maintaining these cycles evolved over the first ca 2.3 Ga of Earth's history in prokaryotes and, through a sequence of events, led to the production of oxygen via the photobiologically catalysed oxidation of water. However, geochemical evidence suggests that there was a delay of several hundred million years before oxygen accumulated in Earth's atmosphere related to changes in the burial efficiency of organic matter and fundamental alterations in the nitrogen cycle. In the latter case, the presence of free molecular oxygen allowed ammonium to be oxidized to nitrate and subsequently denitrified. The interaction between the oxygen and nitrogen cycles in particular led to a negative feedback, in which increased production of oxygen led to decreased fixed inorganic nitrogen in the oceans. This feedback, which is supported by isotopic analyses of fixed nitrogen in sedimentary rocks from the Late Archaean, continues to the present. However, once sufficient oxygen accumulated in Earth's atmosphere to allow nitrification to out-compete denitrification, a new stable electron 'market' emerged in which oxygenic photosynthesis and aerobic respiration ultimately spread via endosymbiotic events and massive lateral gene transfer to eukaryotic host cells, allowing the evolution of complex (i.e. animal) life forms. The resulting network of electron transfers led a gas composition of Earth's atmosphere that is far from thermodynamic equilibrium (i.e. it is an emergent property), yet is relatively stable on geological time scales. The early coevolution of the C, N and O cycles, and the resulting non-equilibrium gaseous by-products can be used as a guide to search for the presence of life on terrestrial planets outside of our Solar System.

Figure 1

Plot of the abundance of elements in the first three rows of the periodic table relative to H. The six major elements that comprise life on Earth are highlighted.

Figure 2

Schematic of the nitrogen cycle including a scale to show oxidation state. Nitrogen species and arrows in bold are the N cycle that was probably operating before the production of O₂ began in the Late Archaean. With the onset of oxygenic photosynthesis at the end of the Archaean, nitrification and denitrification closed the N cycle allowing the return of fixed N to the atmosphere. The anammox process is included (in grey), although it is not known when in geological history, it became widespread.

Figure 3

(a,b) Variations in Δ³³S and δ¹⁵N for the first 2.5 Ga of sedimentary isotope records that include the Archaean and the Palaeoproterozoic. The Archaean saw the start of life and the initiation of modern plate tectonics; it ended at the great oxidation event. Deviations from zero of Δ³³S indicate mass-independent fraction of S isotopes and the absence of UV shielding ozone in the atmosphere and disappear after 2.5 Ga (see Kaufman et al. 2007). The increase in the minimum value of δ¹⁵N through the Early and Middle Archaean, which probably reflects the least altered values of δ¹⁵N, indicates changes in seawater fixed N–δ¹⁵N arising from seafloor weathering and initiation of oxygenic photosynthesis and nitrification–denitrification processes. Data from Hayes et al. (1983), Sano & Pillinger (1990), Pinti & Hashizume (2001), Hu et al. (2003), Mosjzsis et al. (2003), Ono et al. (2003, 2006), Jia & Kerrich (2004), Bekker et al. (2004), Johnston et al. (2005), Papineau et al. (2005), Ohmoto et al. (2006) and Kaufman et al. (2007).