The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis

Abstract

The evolution of O(2)-producing cyanobacteria that use water as terminal reductant transformed Earth's atmosphere to one suitable for the evolution of aerobic metabolism and complex life. The innovation of water oxidation freed photosynthesis to invade new environments and visibly changed the face of the Earth. We offer a new hypothesis for how this process evolved, which identifies two critical roles for carbon dioxide in the Archean period. First, we present a thermodynamic analysis showing that bicarbonate (formed by dissolution of CO(2)) is a more efficient alternative substrate than water for O(2) production by oxygenic phototrophs. This analysis clarifies the origin of the long debated "bicarbonate effect" on photosynthetic O(2) production. We propose that bicarbonate was the thermodynamically preferred reductant before water in the evolution of oxygenic photosynthesis. Second, we have examined the speciation of manganese(II) and bicarbonate in water, and find that they form Mn-bicarbonate clusters as the major species under conditions that model the chemistry of the Archean sea. These clusters have been found to be highly efficient precursors for the assembly of the tetramanganese-oxide core of the water-oxidizing enzyme during biogenesis. We show that these clusters can be oxidized at electrochemical potentials that are accessible to anoxygenic phototrophs and thus the most likely building blocks for assembly of the first O(2) evolving photoreaction center, most likely originating from green nonsulfur bacteria before the evolution of cyanobacteria.

Figure 1

Standard free energy differences and chemical equilibria in pure water and in a two-component system of water and CO₂. Energies are in kcal/mol. Data from NIST sources (http://webbook.nist.gov/chemistry) (42).

Figure 2

Standard reduction potentials [volts vs. NHE normal hydrogen electrode)] per electron for oxidation of water, aqueous bicarbonate, the 1:2 dimanganese/bicarbonate complex, Mn₂(HCO₃)₄, and the photooxidizable reaction center pigment found in cyanobacteria and higher plants (P680; Chl-a), purple bacteria and green bacteria (P870; BChl-a), and heliobacteria (P798; BChl-g) (31). Energies of the excited states (P*) are in electron volts.

Figure 3

Representative electrochemical data for the reduction of a solution of Mn^II (2.5 × 10⁻⁴ M MnSO₄) to Mn⁰ at a Hg electrode as a function of the concentration of bicarbonate (pH 8.3, 0.1 M LiCLO₄). Voltage scanning at 50 mV s⁻¹. Inset shows the standard reduction potentials and formulas of the Mn^II species that form.

Figure 4

Titration of the EPR signal intensities as function of bicarbonate concentration for the Mn^II_aq species (g2 six-line spectrum, Inset) and the broad signal that replaces it upon addition of bicarbonate (broad signal, Inset). The broad signal is detectable only below 70 K, and it exhibits strong spin relaxation and a temperature-dependent linewidth and a g value indicative of formation of a Mn^II_x-bicarbonate oligomer.

Figure 5

(Lower) Proposed evolutionary stages of development of type II bacterial reaction centers towards cyanobacterial (oxygen-evolving) reaction centers in the Archean period. (Upper) Electrochemical potentials of the reaction center photooxidant (P) and terminal substrates (D = formate, oxalate, etc.).