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

G Charles Dismukes, V. V. Klimov, S. V. Baranov, Yu N. Kozlov, J. DasGupta, A. Tyryshkin

Research output: Contribution to journalArticle

205 Citations (Scopus)

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 CO2) is a more efficient alternative substrate than water for O2 production by oxygenic phototrophs. This analysis clarifies the origin of the long debated "bicarbonate effect" on photosynthetic O2 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 O2 evolving photore-action center, most likely originating from green nonsulfur bacteria before the evolution of cyanobacteria.

Original languageEnglish
Pages (from-to)2170-2175
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume98
Issue number5
DOIs
Publication statusPublished - Feb 27 2001

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Photosynthesis
Bicarbonates
Oxygen
Water
Reducing Agents
Cyanobacteria
Chloroflexi
Manganese
Atmosphere
Thermodynamics
Carbon Dioxide
Oceans and Seas
Oxides
Enzymes

Keywords

  • Bicarbonate
  • Carbon dioxide
  • Cyanobacteria
  • Evolution
  • Manganese

ASJC Scopus subject areas

  • Genetics
  • General

Cite this

The origin of atmospheric oxygen on Earth : The innovation of oxygenic photosynthesis. / Dismukes, G Charles; Klimov, V. V.; Baranov, S. V.; Kozlov, Yu N.; DasGupta, J.; Tyryshkin, A.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 98, No. 5, 27.02.2001, p. 2170-2175.

Research output: Contribution to journalArticle

Dismukes, G Charles ; Klimov, V. V. ; Baranov, S. V. ; Kozlov, Yu N. ; DasGupta, J. ; Tyryshkin, A. / The origin of atmospheric oxygen on Earth : The innovation of oxygenic photosynthesis. In: Proceedings of the National Academy of Sciences of the United States of America. 2001 ; Vol. 98, No. 5. pp. 2170-2175.
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