The age of Rubisco: the evolution of oxygenic photosynthesis

The evolutionary history of oxygenesis is controversial. Form I of ribulose 1,5‐bisphosphate carboxylase/oxygenase (Rubisco) in oxygen‐tolerant organisms both enables them to carry out oxygenic extraction of carbon from air and enables the competitive process of photorespiration. Carbon isotopic evidence is presented from ~2.9 Ga stromatolites from Steep Rock, Ontario, Canada, ~2.9 Ga stromatolites from Mushandike, Zimbabwe, and ~2.7 Ga stromatolites in the Belingwe belt, Zimbabwe. The data imply that in all three localities the reef‐building autotrophs included organisms using Form I Rubisco. This inference, though not conclusive, is supported by other geochemical evidence that these stromatolites formed in oxic conditions. Collectively, the implication is that oxygenic photosynthesizers first appeared ~2.9 Ga ago, and were abundant 2.7–2.65 Ga ago. Rubisco specificity (its preference for CO₂ over O₂) and compensation constraints (the limits on carbon fixation) may explain the paradox that despite the inferred evolution of oxygenesis 2.9 Ga ago, the Late Archaean air was anoxic. The atmospheric CO₂:O₂ ratio, and hence greenhouse warming, may reflect Form I Rubisco's specificity for CO₂ over O₂. The system may be bistable under the warming Sun, with liquid oceans occurring in either anoxic (H₂O with abundant CH₄ plus CO₂) or oxic (H₂O with more abundant CO₂, but little CH₄) greenhouse states. Transition between the two states would involve catastrophic remaking of the biosphere. Build‐up of a very high atmospheric inventory of CO₂ in the 2.3 Ga glaciation may have allowed the atmosphere to move up the CO₂ compensation line to reach stability in an oxygen‐rich system. Since then, Form I Rubisco specificity and consequent compensation limits may have maintained the long‐term atmospheric disproportion between O₂ and CO₂, which is now close to both CO₂ and O₂ compensation barriers.