Skip to main content
SpringerLink
Log in

Origin of Oxygenic Photosynthesis from Anoxygenic Type I and Type II Reaction Centers

  • Chapter
  • First Online:
The Biophysics of Photosynthesis

Part of the book series: Biophysics for the Life Sciences ((BIOPHYS,volume 11))

  • 2388 Accesses

Abstract

All anoxygenic photosynthetic bacteria currently known have photosynthetic reaction centers of only one type, either type I or II. In contrast, all oxygenic photosynthetic systems—of plants, algae, and cyanobacteria—have both type I and type II reaction centers. Molecular oxygen is the oxidation product of water in a type II reaction center that is connected, in series, with a type I reaction center. Around 2.4 billion years ago, the evolutionary origin of this series connection initiated biological water oxidation and began to transform our planet irrevocably. Here I consider the question of how separate type I and type II reaction centers diverged from a common ancestor. How they later became linked together, to become interdependent, is also considered, and an answer proposed. The “redox switch hypothesis” for the first cyanobacterium envisages an evolutionary precursor in which type I and type II reaction center genes are present in the genome of a single anoxygenic bacterial lineage, but never expressed at the same time, their gene products forming different reaction centers for light energy conversion under different growth conditions. I suggest that mutation disrupting redox control allowed these two reaction centers to coexist—an arrangement selected against prior to the acquisition of a catalyst of water oxidation while having a selective advantage thereafter. Predictions of this hypothesis include a modern, anoxygenic descendent of the proto-cyanobacterium whose disabled redox switch triggered the Great Oxidation Event, transforming both biology and Earth’s surface geochemistry.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 119.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 159.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 159.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Witt HT. Coupling of quanta, electrons, fields, ions and phosphorylation in the functional membrane of photosynthesis. Results by pulse spectroscopic methods. [Review]. Q Rev Biophys. 1971;4(4):365–477.

    Article  Google Scholar 

  2. Hill R, Bendall F. Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature. 1960;186(4719):136–7.

    Article  ADS  Google Scholar 

  3. Johnston DT, Wolfe-Simon F, Pearson A, Knoll AH. Anoxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth’s middle age. Proc Natl Acad Sci U S A. 2009;106(40):16925–9.

    Article  ADS  Google Scholar 

  4. Nitschke W, Rutherford AW. Photosynthetic reaction centres: variations on a common structural theme? Trends Biochem Sci. 1991;16(7):241–5.

    Article  Google Scholar 

  5. Cardona T, Sedoud A, Cox N, Rutherford AW. Charge separation in photosystem II: a comparative and evolutionary overview. BBA Bioenerg. 2012;1817(1):26–43.

    Article  Google Scholar 

  6. Hohmann-Marriott MF, Blankenship RE. Evolution of photosynthesis. Annu Rev Plant Biol. 2011;62:515–48.

    Article  Google Scholar 

  7. Rutherford AW, Osyczka A, Rappaport F. Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O-2. FEBS Lett. 2012;586(5):603–16.

    Article  Google Scholar 

  8. Saito K, Rutherford AW, Ishikita H. Mechanism of proton-coupled quinone reduction in photosystem II. Proc Natl Acad Sci U S A. 2013;110(3):954–9.

    Article  ADS  Google Scholar 

  9. Deisenhofer J, Epp O, Miki K, Huber R, Michel H. Structure of the protein subunits in the photosynthetic reaction center of rhodopseudomonas-viridis at 3a resolution. Nature. 1985;318(6047):618–24.

    Article  ADS  Google Scholar 

  10. Deisenhofer J, Michel H, Huber R. The structural basis of photosynthetic light reactions in bacteria. Trends Biochem Sci. 1985;10(6):243–8.

    Article  Google Scholar 

  11. Schubert WD, Klukas O, Saenger W, Witt HT, Fromme P, Krauss N. A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. J Mol Biol. 1998;280(2):297–314.

    Article  Google Scholar 

  12. Amunts A, Drory O, Nelson N. The structure of a plant photosystem I supercomplex at 3.4 A resolution. Nature. 2007;58–63.

    Google Scholar 

  13. Ben-Shem A, Frolow F, Nelson N. Crystal structure of plant photosystem I. Nature. 2003;426(6967):630–5.

    Article  ADS  Google Scholar 

  14. Hauska G, Schoedl T, Remigy H, Tsiotis G. The reaction center of green sulfur bacteria. BBA Bioenerg. 2001;1507(1–3):260–77.

    Article  Google Scholar 

  15. Umena Y, Kawakami K, Shen JR, Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 angstrom. Nature. 2011;473(7345):55–U65.

    Article  ADS  Google Scholar 

  16. Raymond J, Blankenship RE. The evolutionary development of the protein complement of photosystem 2. BBA Bioenerg. 2004;1655(1–3):133–9.

    Article  Google Scholar 

  17. Baymann D, Brugna M, Muhlenhoff U, Nitschke W. Daddy, where did (PS)I come from? BBA Bioenerg. 2001;1507(1–3):291–310.

    Article  Google Scholar 

  18. Xiong J, Fischer WM, Inoue K, Nakahara M, Bauer CE. Molecular evidence for the early evolution of photosynthesis. Science. 2000;289(5485):1724–30.

    Article  ADS  Google Scholar 

  19. Hall DO, Cammack R, Rao KK. Role for ferredoxins in origin of life and biological evolution. Nature. 1971;233(5315):136.

    Article  ADS  Google Scholar 

  20. Russell MJ, Allen JF, Milner-White EJ. Inorganic complexes enabled the onset of life and oxygenic photosynthesis. In: Allen JF, Gantt E, Golbeck JH, Osmond B, editors. Photosynthesis 2007 Energy from the Sun Proceedings of the 14th international congress on photosynthesis. Heidelberg: Springer; 2008. p. 1187–92.

    Google Scholar 

  21. Bauer C, Elsen S, Swem LR, Swem DL, Masuda S. Redox and light regulation of gene expression in photosynthetic prokaryotes. Phil Trans Roy Soc Lond B. 2003;358(1429):147–54.

    Article  Google Scholar 

  22. Marrs BL. Molecular-genetics studies of gene-expression and protein-structure function relationships in photosynthetic bacteria. FEMS Symp. 1990;53:1–4.

    Google Scholar 

  23. Allen JF. Redox homeostasis in the emergence of life. On the constant internal environment of nascent living cells. J Cosmol. 2010;10:3362–73.

    Google Scholar 

  24. Hill R, Bendall F. Function of the two cytochrome components in chloroplasts - a working hypothesis. Nature. 1960;186(4719):136–7.

    Article  ADS  Google Scholar 

  25. Myers J. Enhancement studies in photosynthesis. Ann Rev Plant Physio. 1971;22:289.

    Article  Google Scholar 

  26. Allen JF, Bennett J, Steinback KE, Arntzen CJ. Chloroplast protein-phosphorylation couples plastoquinone redox state to distribution of excitation-energy between photosystems. Nature. 1981;291(5810):25–9.

    Article  ADS  Google Scholar 

  27. Pfannschmidt T, Nilsson A, Allen JF. Photosynthetic control of chloroplast gene expression. Nature. 1999;397(6720):625–8.

    Article  ADS  Google Scholar 

  28. Allen JF, Santabarbara S, Allen CA, Puthiyaveetil S. Discrete redox signaling pathways regulate photosynthetic light-harvesting and chloroplast gene transcription. PLoS One. 2011;6(10):e26372.

    Article  ADS  Google Scholar 

  29. Allen JF, Pfannschmidt T. Balancing the two photosystems: photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts. Phil Trans Roy Soc Lond Ser B Biol Sci. 2000;355(1402):1351–7.

    Google Scholar 

  30. Nisbet EG, Sleep NH. The habitat and nature of early life. Nature. 2001;409(6823):1083–91.

    Article  ADS  Google Scholar 

  31. Mazor Y, Greenberg I, Toporik H, Beja O, Nelson N. The evolution of photosystem I in light of phage-encoded reaction centres. Phil Trans Roy Soc B Biol Sci. 2012;367(1608):3400–5.

    Article  Google Scholar 

  32. Olson JM, Blankenship RE. Thinking about the evolution of photosynthesis. Photosynth Res. 2004;80(1–3):373–86.

    Article  Google Scholar 

  33. Olson JM, Pierson BK. Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol. 1987;108:209–48.

    Article  Google Scholar 

  34. Arnon DI, Chain RK. Role of oxygen in ferredoxin-catalyzed cyclic photophosphorylations. FEBS Lett. 1977;82(2):297–302.

    Article  Google Scholar 

  35. Allen JF. Photosynthesis of ATP-electrons, proton pumps, rotors, and poise. Cell. 2002;110(3):273–6.

    Article  Google Scholar 

  36. Allen JF. Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci. 2003;8(1):15–9.

    Article  Google Scholar 

  37. Allen JF. Oxygen reduction and optimum production of Atp in photosynthesis. Nature. 1975;256(5518):599–600.

    Article  ADS  Google Scholar 

  38. Blankenship RE, Madigan MT, Bauer CE. Anoxygenic photosynthetic bacteria. Dordrecht: Kluwer; 1995.

    Google Scholar 

  39. Pierson BK, Castenholz RW. Ecology of thermophilic anoxygenic phototrophs. In: Blankenship RE, Madigan MT, Bauer CE, editors. Anoxygenic photosynthetic bacteria. Dordrecht: Kluwer; 1995. p. 87–103.

    Google Scholar 

  40. Johnston DT, Poulton SW, Fralick PW, Wing BA, Canfield DE, Farquhar J. Evolution of the oceanic sulfur cycle at the end of the Paleoproterozoic. Geochim Cosmochim Acta. 2006;70(23):5723–39.

    Article  ADS  Google Scholar 

  41. Li H, Sherman LA. A redox-responsive regulator of photosynthesis gene expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol. 2000;182(15):4268–77.

    Article  Google Scholar 

  42. Eraso JM, Kaplan S. From redox flow to gene regulation: role of the PrrC protein of Rhodobacter sphaeroides 2.4.1. Biochemistry. 2000;39(8):2052–62.

    Article  Google Scholar 

  43. Wu J, Bauer CE. RegB kinase activity is controlled in part by monitoring the ratio of oxidized to reduced ubiquinones in the ubiquinone pool. MBio. 2010;1(5):e00272–10.

    Article  Google Scholar 

  44. Georgellis D, Kwon O, Lin EC. Quinones as the redox signal for the ARC two-component system of bacteria. Science. 2001;292(5525):2314–6.

    Article  Google Scholar 

  45. Green J, Scott C, Guest JR. Functional versatility in the CRP-FNR superfamily of transcription factors: FNR and FLP. Adv Microb Physiol. 2001;44:1–34.

    Article  Google Scholar 

  46. Unden G, Bongaerts J. Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta Bioenerg. 1997;1320(3):217–34.

    Article  Google Scholar 

  47. Alexeeva S, Hellingwerf KJ, Teixeira de Mattos MJ. Requirement of ArcA for redox regulation in Escherichia coli under microaerobic but not anaerobic or aerobic conditions. J Bacteriol. 2003;185(1):204–9.

    Article  Google Scholar 

  48. Oren A, Padan E. Induction of anaerobic, photoautotrophic growth in the cyanobacterium Oscillatoria limnetica. J Bacteriol. 1978;133(2):558–63.

    Google Scholar 

  49. Sauer K, Yachandra VK. A possible evolutionary origin for the Mn4 cluster of the photosynthetic water oxidation complex from natural MnO2 precipitates in the early ocean. Proc Natl Acad Sci U S A. 2002;99(13):8631–6.

    Article  ADS  Google Scholar 

  50. Dismukes GC, Klimov VV, Baranov SV, Kozlov YN, DasGupta J, Tyryshkin A. Special feature: the origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci U S A. 2001;98(5):2170–5.

    Article  ADS  Google Scholar 

  51. Khorobrykh A, Dasgupta J, Kolling DRJ, Terentyev V, Klimov VV, Dismukes GC. Evolutionary origins of the photosynthetic water oxidation cluster: bicarbonate permits Mn2+ photo-oxidation by anoxygenic bacterial reaction centers. Chembiochem. 2013;14(14):1725–31.

    Article  Google Scholar 

  52. Allen JF, Martin W. Evolutionary biology - out of thin air. Nature. 2007;445(7128):610–2.

    Article  Google Scholar 

  53. Cheniae GM. Photosystem-II and O2 evolution. Ann Rev Plant Physio. 1970;21:467.

    Article  Google Scholar 

  54. Allen JP, Olson TL, Oyala P, Lee WJ, Tufts AA, Williams JC. Light-driven oxygen production from superoxide by Mn-binding bacterial reaction centers. Proc Natl Acad Sci U S A. 2012;109(7):2314–8.

    Article  ADS  Google Scholar 

  55. Johnson JE, Webb SM, Thomas K, Ono S, Kirschvink JL, Fischer WW. Manganese-oxidizing photosynthesis before the rise of cyanobacteria. Proc Natl Acad Sci. 2013;110(28):11238–43.

    Article  ADS  Google Scholar 

  56. Kalman L, LoBrutto R, Allen JP, Williams JC. Manganese oxidation by modified reaction centers from Rhodobacter sphaeroides. Biochemistry. 2003;42(37):11016–22.

    Article  Google Scholar 

  57. Rutherford AW, Boussac A. Biochemistry. Water photolysis in biology. Science. 2004;303(5665):1782–4.

    Article  Google Scholar 

  58. Rutherford AW, Faller P. Photosystem II: evolutionary perspectives. Philos Trans R Soc Lond B Biol Sci. 2003;358(1429):245–53.

    Article  Google Scholar 

  59. Allen JF. A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Lett. 2005;579(5):963–8.

    Article  Google Scholar 

  60. Allen JF, Puthiyaveetil S. Chloroflexus aurantiacus and the origin of oxygenic, two-light reaction photosynthesis in failure to switch between type I and type II reaction centres. In: van der Est A, Bruce D, editors. Photosynthesis: fundamental aspects to global perspectives. Lawrence, KS: Alliance Communications Group; 2005. p. 455–7.

    Google Scholar 

  61. Lane N. Oxygen. Oxford: Oxford University Press; 2002.

    Google Scholar 

  62. Tang KH, Barry K, Chertkov O, Dalin E, Han CS, Hauser LJ, et al. Complete genome sequence of the filamentous anoxygenic phototrophic bacterium Chloroflexus aurantiacus. BMC Genomics. 2011;29:12.

    Google Scholar 

  63. Arieli B, Padan E, Shahak Y. Sulfide-induced sulfide-quinone reductase activity in thylakoids of Oscillatoria limnetica. J Biol Chem. 1991;266(1):104–11.

    Google Scholar 

  64. Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, et al. The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc Natl Acad Sci U S A. 2008;105(29):10061–6.

    Article  ADS  Google Scholar 

  65. Sousa FL, Shavit-Grievink L, Allen JF, Martin WF. Chlorophyll biosynthesis gene evolution indicates photosystem gene duplication, not photosystem merger, at the origin of oxygenic photosynthesis. Genome Biol Evol. 2013;5(1):200–16.

    Article  Google Scholar 

  66. Dagan T, Roettger M, Stucken K, Landan G, Koch R, Major P, et al. Genomes of stigonematalean cyanobacteria (subsection v) and the evolution of oxygenic photosynthesis from prokaryotes to plastids. Genome Biol Evol. 2013;5(1):31–44.

    Article  Google Scholar 

  67. Macalady JL, Schaperdoth I, Fulton JM, Freeman KH, Hanson TE. Microbial biogeochemistry of a meromictic blue hole. Geochim Cosmochim Acta. 2010;74(12):A651.

    Google Scholar 

  68. Maresca JA, Crowe SA, Macalady JL. Anaerobic photosynthetic ecosystems. Geobiology. 2012;10(3):193–5.

    Article  Google Scholar 

  69. Gonzalez BC, Iliffe TM, Macalady JL, Schaperdoth I, Kakuk B. Microbial hotspots in anchialine blue holes: initial discoveries from the Bahamas. Hydrobiologia. 2011;677(1):149–56.

    Article  Google Scholar 

  70. Sahl JW, Gary MO, Harris JK, Spear JR. A comparative molecular analysis of water-filled limestone sinkholes in north-eastern Mexico. Environ Microbiol. 2011;13(1):226–40.

    Article  Google Scholar 

  71. Dietrich LEP, Tice MM, Newman DK. The co-evolution of life and Earth. Curr Biol. 2006;16(11):R395–400.

    Article  Google Scholar 

Download references

Acknowledgements

I thank Nick Lane, William Martin, Wolfgang Nitschke, and Michael Russell for discussions on this and related topics.

Author information

Authors and Affiliations

  1. Research Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK

    John F. Allen Ph.D.

Authors
  1. John F. Allen Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John F. Allen Ph.D. .

Editor information

Editors and Affiliations

  1. Dept of Biochemistry & Molecular Biology, Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania, USA

    John Golbeck

  2. Dept of Chemistry, Brock University, St. Catharines, Ontario, Canada

    Art van der Est

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Allen, J.F. (2014). Origin of Oxygenic Photosynthesis from Anoxygenic Type I and Type II Reaction Centers. In: Golbeck, J., van der Est, A. (eds) The Biophysics of Photosynthesis. Biophysics for the Life Sciences, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1148-6_14

Download citation

Publish with us

Policies and ethics

Search

Navigation