Advertisement

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
ELSI SYMPOSIUM

Abstract

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.

Keywords

Great oxidation event MIF Detrital pyrite PSII WOC Molecular evolution 

Notes

Acknowledgments

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).

References

  1. Allen JF, Martin W (2007) Evolutionary biology: out of thin air. Nature 445:610–612PubMedCrossRefGoogle Scholar
  2. Armstrong FA (2008) Why did Nature choose manganese to make oxygen? Philos Trans R Soc B 363:1263–1270CrossRefGoogle Scholar
  3. Beukes NJ (1987) Facies relations, depositional environments, and diagenesis in a major early Proterozoic stromatolitic carbonate platform to basinal sequence, Campbellrand Subgroup, Transvaal Supergroup, Southern Africa. Sediment Geol 54:1–46CrossRefGoogle Scholar
  4. Blankenship RE, Hartman H (1998) The origin and evolution of oxygenic photosynthesis. Trends Biochem Sci 23:94–97PubMedCrossRefGoogle Scholar
  5. Bryant ZA, Liu Z (2013) Green bacteria: insights into green bacterial evolution through genomic analyses, advances in botanical research. 66, Elsevier Ltd. ISSN 0065–2296, http://dx.doi.org/ 10.1016/B978-0-12-397923-0.00004-7
  6. Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, DasGupta J, Tryshkin A (2001) The origin of atmospheric oxygen on earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci U S A 98:2170–2175PubMedCentralPubMedCrossRefGoogle Scholar
  7. Farquhar J, Bao HM, Thiemens M (2000) Atmospheric influence of Earth’s earliest sulfur cycle. Science 289:756–758PubMedCrossRefGoogle Scholar
  8. Fischer WW, Knoll AH (2009) An iron shuttle for deepwater silica in Late Archean and early Paleoproterozoic iron formation. Geol Soc Am Bull 121:222–235Google Scholar
  9. Fischer WW, Fike DA, Johnson JE, Raub TD, Guan Y, Kirschvink JL, Eiler JM (2014) SQUID-SIMS is a useful approach to uncover primary signals in the Archean sulfur cycle. Proc Natl Acad Sci 111:5468–5473PubMedCentralPubMedCrossRefGoogle Scholar
  10. Frimmel HE (2005) Archaean atmospheric evolution: evidence from the Witwatersrand gold fields. S Afr Earth Sci Rev 70:1–46CrossRefGoogle Scholar
  11. Gould SJ, Vrba ES (1982) Exaptation - a missing term in the science of form. Paleobiology 8:4–15Google Scholar
  12. Granick S (1957) Speculations on the origins and evolution of photosynthesis. Ann N Y Acad Sci 69:292–308PubMedCrossRefGoogle Scholar
  13. Guy BM, Ono S, Gutzmer J, Kaufman AJ, Lin Y, Fogel ML, Beukes NJ (2012) A multiple sulfur and organic carbon isotope record from conglomeratic sedimentary rocks of the Mesoarchean Witwatersrand Supergroup. S Afr Precambrian Res 219:208–231CrossRefGoogle Scholar
  14. Hohmann-Marriott MF, Blankenship RE (2011) The evolution of photosynthesis. Annu Rev Plant Biol 62:515–548PubMedCrossRefGoogle Scholar
  15. Johnson JE, Webb SM, Thomas K, Ono S, Kirschvink JL, Fischer WW (2013a) Manganese-oxidizing photosynthesis before the rise of cyanobacteria. Proc Natl Acad Sci 108:11238–11243CrossRefGoogle Scholar
  16. Johnson JE, Webb SM, Thomas K, Ono S, Kirschvink JL, Fischer WW (2013b) Correcting mistaken views of sedimentary geology, Mn-oxidation rates, and molecular clocks. Proc Natl Acad Sci 110:E4119–E41120PubMedCentralPubMedCrossRefGoogle Scholar
  17. Johnson JE, Gerpheide A, Lamb MP, Fischer WW (2014) O2 constraints from Paleoproterozoic detrital pyrite and uraninite. Geol Soc Am Bull. Published online ahead of print on 27 Feb. 2014, doi:  10.1130/B30949.1
  18. Kappler A, Pasquero C, Konhauser KO, Newman DK (2005) Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria. Geology 33:865–868CrossRefGoogle Scholar
  19. Kharecha P, Kasting J, Siefert J (2005) A coupled atmosphere-ecosystem model of the early Archean Earth. Geobiology 3:53–76CrossRefGoogle Scholar
  20. Klein C (2005) Some Precambrian banded iron-formations (BIFs) from around the world: Their age, geologic setting, mineralogy, metamorphism, geochemistry, and origin. Am Mineral 90:1473–1499. doi: 10.2138/am.2005.1871
  21. Kopp RE, Kirschvink JL, Hilburn IA, Nash CZ (2005) Was the Paleoproterozoic Snowball Earth a biologically-triggered climate disaster? Proc Natl Acad Sci 102:11131–11136PubMedCentralPubMedCrossRefGoogle Scholar
  22. McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483PubMedCrossRefGoogle Scholar
  23. Mix LJ, Haig D, Cavanaugh CM (2005) Phylogenetic analyses of the core antenna domain: investigating the origin of photosystem I. J Mol Evol 60:153–163PubMedCrossRefGoogle Scholar
  24. Morgan JJ (2005) Kinetics of reaction between O2 and Mn(II) species in aqueous solutions. Geochim Cosmochim Acta 69:35–48CrossRefGoogle Scholar
  25. Olson JM (1970) The evolution of photosynthesis. Science 168:438–446PubMedCrossRefGoogle Scholar
  26. Ono S, Beukes NJ, Rumble D, Fogel M (2006) Early evolution of Earth’s atmospheric oxygen from multiple sulfur and carbon isotope records of the 2.9 Ga Pongola Supergroup, Southern Africa. S Afr J Geol 109:97A108CrossRefGoogle Scholar
  27. Pavlov AA, Kasting JF (2002) Mass-independent fractionation of sulfur isotopes in Archean sediments: strong evidence for an anoxic Archean atmosphere. Astrobiology 2:27–41PubMedCrossRefGoogle Scholar
  28. Planavsky NJ, Asael D, Hofmann A, Reinhard CT, Lalonde SV, Knudsen A, Wang X, Ossa Ossa F, Pecoits E, Smith AJB, Beukes NJ, Bekker A, Johnson TM, Konhauser KO, Lyons TW, Rouxel OJ (2014) Evidence for oxygenic photosynthesis half a billion years before the great oxidation event. Nat Geosci 7:283–286CrossRefGoogle Scholar
  29. Ronov AB, Migdisov AA (1971) Evolution of the chemical composition of the rocks in the shields and sediment cover of the Russian and North American Platforms. Sedimentology 16:137–185CrossRefGoogle Scholar
  30. Rutherford W, Faller P (2002) Photosystem II: evolutionary perspectives. Philos Trans R Soc London B 358:245–253CrossRefGoogle Scholar
  31. Sadekar S, Raymond R, Blankenship RE (2006) Conservation of distantly related membrane proteins: photosynthetic reaction centers share a common structural core. Mol Biol Evol 23:2001–2007PubMedCrossRefGoogle Scholar
  32. Schoepp-Cothenet B, Lieutaud C, Baymann F, Vermeglio A, Friedrich T, Kramer DM, Nitschke W (2009) Menaquinone as pool quinone in a purple bacterium. Proc Natl Acad Sci 106:8549–8554PubMedCentralPubMedCrossRefGoogle Scholar
  33. Schröder C, Bedorf D, Beukes NJ, Gutzmer J, (2011) From BIF to red beds: Sedimentology and sequence stratigraphy of the Paleoproterozoic Koegas Subgroup (South Africa). Sediment Geol 236(1–2):25–44. doi: 10.1016/j.sedgeo.2010.11.007
  34. Sekine Y, Tajika E, Tada R, Hirai T, Goto KT, Kuwatani T, Goto K, Yamamoto S, Tachibana S, Isozaki Y, Kirschvink JL (2011) Manganese enrichment in the Gowganda Formation of the Huronian Supergroup: a highly oxidizing shallow-marine environment after the last Huronian glaciation. Earth Planet Sci Lett 307:201–210CrossRefGoogle Scholar
  35. Smith AJB (2007) The Paleoenvironmental Significance of the Iron-formations and Iron-rich Mudstones of the Mesoarchean Witwatersrand-Mozaan Basin, South Africa. UJ Thesis, https://ujdigispace.uj.ac.za/handle/10210/2440
  36. Stumm W, Morgan JJ (1996) Aquatic chemistry: Chemical equilibria and rates in natural waters, 3rd edn. Wiley, New York, p 1042Google Scholar
  37. Sumner DY (1997) Carbonate precipitation and oxygen stratification in Late Archean seawater as deduced from facies and stratigraphy of the Gamohaan and Frisco Formations, Transvaal Supergroup, South Africa. Am J Sci 297:455–487CrossRefGoogle Scholar
  38. Sumner DY, Grotzinger JP (1996) Were kinetics of Archean calcium carbonate precipitation related to oxygen concentration? Geology 24:119–122PubMedCrossRefGoogle Scholar
  39. Sumner DY, Grotzinger JP (2004) Implications for Neoarchaean ocean chemistry from primary carbonate mineralogy of the Campbellrand-Malmani Platform. S Afr Sedimentol 51:1273–1299CrossRefGoogle Scholar
  40. Tamura N, Cheniae G (1987) Photoactivation of the water-oxidizing complex inPhotosystem II membranes depleted of Mn and extrinsic proteins. I. Biochemical andkinetic characterization. Biochim Biophys Acta Bioenerg 890:179–194CrossRefGoogle Scholar
  41. Turekian KK, Wedepohl KH (1961) Distribution of the elements in some major units of the Earth’s crust. Geol Soc Am Bull 72:175–192CrossRefGoogle Scholar
  42. Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen- evolving photosystem II at a resolution of 1.9 A. Nature 473:55–60PubMedCrossRefGoogle Scholar
  43. Veizer J (1985) Carbonates and ancient oceans: Isotopic and chemical record on time scales of 107–109 years. In E. T. Sunquist and W. S. Broecker (eds.) The carbon cycle and atmospheric CO2: Natural variations archean to present. Geophysical Monograph Series, 32, 595–601, AGU.Google Scholar
  44. Veizer J, Hoefs J, Ridler RH, Jensen LS, Lowe DR (1989a) Geochemistry of Precambrian carbonates: I. Archean hydrothermal systems. Geochim Cosmochim Acta 53:845–857CrossRefGoogle Scholar
  45. Veizer J, Hoefs J, Lowe DR, Thurston PC (1989b) Geochemistry of Precambrian carbonates: II. Archean greenstone belts and Archean sea water. Geochim Cosmochim Acta 53:859–871PubMedCrossRefGoogle Scholar
  46. Williford KH, Van Kranendonk MJ, Ushikubo T, Kozdon R, Valley JW (2011) Constraining atmospheric oxygen and seawater sulfate concentrations during Paleoproterozoic glaciation: in situ sulfur three-isotope microanalysis of pyrite from the Turee Creek Group, Western Australia. Geochim Cosmochim Acta 75:5686–5705CrossRefGoogle Scholar
  47. Zubay G (1996) Origins of life on the earth and in the cosmos, 2nd edn. Academic, San DiegoGoogle Scholar

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

Personalised recommendations