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

Abstract

The evolution of O2-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 Mnbicarbonate 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.bicarbonate ͉ carbon dioxide ͉ cyanobacteria ͉ evolution ͉ manganese O xygen (O 2 ) production by photosynthesis is by far the dominant global process that replenishes atmospheric and oceanic oxygen essential to sustain all aerobic life. Geochemical records of terrestrial oxides indicate that O 2 evolution must have taken place in the precursors to cyanobacteria before ca. 2.8 billion years ago and led to the accumulation of O 2 in the atmosphere (1, 2). The creation of a photosynthetic apparatus capable of splitting water into O 2 , protons, and electrons was the pivotal innovation in the evolution of life on Earth. For the first time photosynthesis had an unlimited source of electrons and protons by using water as reductant. By freeing photosynthesis from the availability of reduced chemical substances, the global production of organic carbon could be enormously increased and opened new environments for photosynthesis to occur. This event literally changed the face of the Earth. The accumulation of O 2 in the atmosphere led to the biological innovation of aerobic respiration, which harnesses a more powerful metabolic energy source. Because aerobic metabolism generates 18 times more energy (ATP) per metabolic input (hexose sugar) than does anaerobic metabolism, the engine of life became supercharged. This sequence of evolutionary steps enabled the emergence of complex, multicellular, energy-efficient, eukaryotic organisms.Comparisons of cyanobacteria, green algae, ...

Dating the cyanobacterial ancestor of the chloroplast

“…After the evolution of life, the second major event that transformed the biogeochemistry of the Earth, was oxygen-evolving photosynthesis by cyanobacteria 2,[17][18][19] .…”

Photoassembly of the water-oxidizing complex in photosystem II

“…Importantly, the photooxidation of the next Mn2+ is catalyzed by formation of the first [Mn 3+ (OH − )] 2+ photoproduct, as the resulting OH − can serve as a better ligand than water to template the binding of the next Mn 2+ . The efficiency of this assembly process increases in the presence of bicarbonate which is a surrogate for hydroxide and can exist in neutral pH solutions at concentrations many orders of magnitude higher than hydroxide [13,57]. 2+ is an essential ion in the photoassembly reaction in all native PSIIWOCs examined to date.…”

“…Their results provide the first evidence that a stable Mn 3+ binding site can be formed in a bacterial reaction center. This suggests a feasible route for evolution of a primitive precursor to the Mn 4 Ca core found universally in contemporary oxygenic reaction centers [13,57]. Construction of biological-inspired completely abiotic synthetic representations of the PSII protein scaffolding and catalytic WOC site are underway in some laboratories [99].…”

Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses

“…Aerobic life is responsible for the major portion of oxygen turnover, with photosynthesis being the main input into the oxygen reservoir, and respiration the main output. The two processes are in approximate equilibrium, and fossil fuel combustion is the major source of oxygen loss from the reservoir (10,11).…”