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Manganese and the Evolution of Photosynthesis

Fischer, Woodward W. and Hemp, James and Johnson, Jena E. (2015) Manganese and the Evolution of Photosynthesis. Origins of Life and Evolution of Biospheres, 45 (3). pp. 351-357. ISSN 0169-6149. doi:10.1007/s11084-015-9442-5.

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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 Mn^(2+), and ultimately water.

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Fischer, Woodward W.0000-0002-8836-3054
Hemp, James0000-0001-7193-0553
Additional Information:© 2015 Springer Science+Business Media Dordrecht. Received: 31 August 2014; Accepted: 24 November 2014. Published online: 29 May 2015. Paper presented at the 2nd Annual Earth-Life Science Institute International Symposium, held at the National Institute of Informatics in Chiyoda-ku, Tokyo, from 24 to 26 March, 2014. 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).
Group:Caltech Center for Environmental Microbial Interactions (CEMI)
Funding AgencyGrant Number
Agouron InstituteUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
NSF Graduate Research FellowshipUNSPECIFIED
Caltech Center for Environmental Microbial Interactions (CEMI)UNSPECIFIED
Subject Keywords:Great oxidation event; MIF; Detrital pyrite; PSII; WOC; Molecular evolution
Issue or Number:3
Record Number:CaltechAUTHORS:20150602-140446953
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:57943
Deposited By: Tony Diaz
Deposited On:02 Jun 2015 21:14
Last Modified:10 Nov 2021 21:57

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