Origins of Life and Evolution of Biospheres

, Volume 45, Issue 3, pp 351–357 | Cite as

Manganese and the Evolution of Photosynthesis

  • Woodward W. FischerEmail author
  • James Hemp
  • Jena E. Johnson


Oxygenic photosynthesis is the most important bioenergetic event in the history of our planet—it evolved once within the Cyanobacteria, and remained largely unchanged as it was transferred to algae and plants via endosymbiosis. Manganese plays a fundamental role in this history because it lends the critical redox behavior of the water-oxidizing complex of photosystem II. Constraints from the photoassembly of the Mn-bearing water-oxidizing complex fuel the hypothesis that Mn(II) once played a key role as an electron donor for anoxygenic photosynthesis prior to the evolution of oxygenic photosynthesis. Here we review the growing body of geological and geochemical evidence from the Archean and Paleoproterozoic sedimentary records that supports this idea and demonstrates that the oxidative branch of the Mn cycle switched on prior to the rise of oxygen. This Mn-oxidizing phototrophy hypothesis also receives support from the biological record of extant phototrophs, and can be made more explicit by leveraging constraints from structural biology and biochemistry of photosystem II in Cyanobacteria. These observations highlight that water-splitting in photosystem II evolved independently from a homodimeric ancestral type II reaction center capable of high potential photosynthesis and Mn(II) oxidation, which is required by the presence of homologous redox-active tyrosines in the modern heterodimer. The ancestral homodimer reaction center also evolved a C-terminal extension that sterically precluded standard phototrophic electron donors like cytochrome c, cupredoxins, or high-potential iron-sulfur proteins, and could only complete direct oxidation of small molecules like Mn2+, and ultimately water.


Great oxidation event MIF Detrital pyrite PSII WOC Molecular evolution 



We extend our sincere thanks to Joe Kirschvink, Yuichiro Ueno, Jim Cleaves, and others from the Earth-Life Science Institute for their support and organization of the 2nd International ELSI symposium where we presented this work. Funding for this work was graciously provided by the Agouron Institute (WWF and JH), Packard Foundation (WWF), National Science Foundation Graduate Research Fellowship Program (JEJ), and the Caltech Center for Environment-Microbe Interactions (WWF).


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Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Woodward W. Fischer
    • 1
    Email author
  • James Hemp
    • 1
  • Jena E. Johnson
    • 1
  1. 1.Division of Geological and Planetary SciencesCalifornia Institute of TechnologyPasadenaUSA

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