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

  • John F. AllenEmail author
Chapter
Part of the Biophysics for the Life Sciences book series (BIOPHYS, volume 11)

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.

Keywords

Electron transport Photochemistry Evolution Molecular oxygen Redox switch hypothesis Gene expression Biogeochemistry 

Notes

Acknowledgements

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

References

  1. 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.CrossRefGoogle Scholar
  2. 2.
    Hill R, Bendall F. Function of the two cytochrome components in chloroplasts: a working hypothesis. Nature. 1960;186(4719):136–7.CrossRefADSGoogle Scholar
  3. 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.CrossRefADSGoogle Scholar
  4. 4.
    Nitschke W, Rutherford AW. Photosynthetic reaction centres: variations on a common structural theme? Trends Biochem Sci. 1991;16(7):241–5.CrossRefGoogle Scholar
  5. 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.CrossRefGoogle Scholar
  6. 6.
    Hohmann-Marriott MF, Blankenship RE. Evolution of photosynthesis. Annu Rev Plant Biol. 2011;62:515–48.CrossRefGoogle Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.CrossRefADSGoogle Scholar
  9. 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.CrossRefADSGoogle Scholar
  10. 10.
    Deisenhofer J, Michel H, Huber R. The structural basis of photosynthetic light reactions in bacteria. Trends Biochem Sci. 1985;10(6):243–8.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. 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. 13.
    Ben-Shem A, Frolow F, Nelson N. Crystal structure of plant photosystem I. Nature. 2003;426(6967):630–5.CrossRefADSGoogle Scholar
  14. 14.
    Hauska G, Schoedl T, Remigy H, Tsiotis G. The reaction center of green sulfur bacteria. BBA Bioenerg. 2001;1507(1–3):260–77.CrossRefGoogle Scholar
  15. 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.CrossRefADSGoogle Scholar
  16. 16.
    Raymond J, Blankenship RE. The evolutionary development of the protein complement of photosystem 2. BBA Bioenerg. 2004;1655(1–3):133–9.CrossRefGoogle Scholar
  17. 17.
    Baymann D, Brugna M, Muhlenhoff U, Nitschke W. Daddy, where did (PS)I come from? BBA Bioenerg. 2001;1507(1–3):291–310.CrossRefGoogle Scholar
  18. 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.CrossRefADSGoogle Scholar
  19. 19.
    Hall DO, Cammack R, Rao KK. Role for ferredoxins in origin of life and biological evolution. Nature. 1971;233(5315):136.CrossRefADSGoogle Scholar
  20. 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. 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.CrossRefGoogle Scholar
  22. 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. 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. 24.
    Hill R, Bendall F. Function of the two cytochrome components in chloroplasts - a working hypothesis. Nature. 1960;186(4719):136–7.CrossRefADSGoogle Scholar
  25. 25.
    Myers J. Enhancement studies in photosynthesis. Ann Rev Plant Physio. 1971;22:289.CrossRefGoogle Scholar
  26. 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.CrossRefADSGoogle Scholar
  27. 27.
    Pfannschmidt T, Nilsson A, Allen JF. Photosynthetic control of chloroplast gene expression. Nature. 1999;397(6720):625–8.CrossRefADSGoogle Scholar
  28. 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.CrossRefADSGoogle Scholar
  29. 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. 30.
    Nisbet EG, Sleep NH. The habitat and nature of early life. Nature. 2001;409(6823):1083–91.CrossRefADSGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. 32.
    Olson JM, Blankenship RE. Thinking about the evolution of photosynthesis. Photosynth Res. 2004;80(1–3):373–86.CrossRefGoogle Scholar
  33. 33.
    Olson JM, Pierson BK. Evolution of reaction centers in photosynthetic prokaryotes. Int Rev Cytol. 1987;108:209–48.CrossRefGoogle Scholar
  34. 34.
    Arnon DI, Chain RK. Role of oxygen in ferredoxin-catalyzed cyclic photophosphorylations. FEBS Lett. 1977;82(2):297–302.CrossRefGoogle Scholar
  35. 35.
    Allen JF. Photosynthesis of ATP-electrons, proton pumps, rotors, and poise. Cell. 2002;110(3):273–6.CrossRefGoogle Scholar
  36. 36.
    Allen JF. Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci. 2003;8(1):15–9.CrossRefGoogle Scholar
  37. 37.
    Allen JF. Oxygen reduction and optimum production of Atp in photosynthesis. Nature. 1975;256(5518):599–600.CrossRefADSGoogle Scholar
  38. 38.
    Blankenship RE, Madigan MT, Bauer CE. Anoxygenic photosynthetic bacteria. Dordrecht: Kluwer; 1995.Google Scholar
  39. 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. 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.CrossRefADSGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.CrossRefGoogle Scholar
  46. 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.CrossRefGoogle Scholar
  47. 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.CrossRefGoogle Scholar
  48. 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. 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.CrossRefADSGoogle Scholar
  50. 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.CrossRefADSGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 52.
    Allen JF, Martin W. Evolutionary biology - out of thin air. Nature. 2007;445(7128):610–2.CrossRefGoogle Scholar
  53. 53.
    Cheniae GM. Photosystem-II and O2 evolution. Ann Rev Plant Physio. 1970;21:467.CrossRefGoogle Scholar
  54. 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.CrossRefADSGoogle Scholar
  55. 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.CrossRefADSGoogle Scholar
  56. 56.
    Kalman L, LoBrutto R, Allen JP, Williams JC. Manganese oxidation by modified reaction centers from Rhodobacter sphaeroides. Biochemistry. 2003;42(37):11016–22.CrossRefGoogle Scholar
  57. 57.
    Rutherford AW, Boussac A. Biochemistry. Water photolysis in biology. Science. 2004;303(5665):1782–4.CrossRefGoogle Scholar
  58. 58.
    Rutherford AW, Faller P. Photosystem II: evolutionary perspectives. Philos Trans R Soc Lond B Biol Sci. 2003;358(1429):245–53.CrossRefGoogle Scholar
  59. 59.
    Allen JF. A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Lett. 2005;579(5):963–8.CrossRefGoogle Scholar
  60. 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. 61.
    Lane N. Oxygen. Oxford: Oxford University Press; 2002.Google Scholar
  62. 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. 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. 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.CrossRefADSGoogle Scholar
  65. 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.CrossRefGoogle Scholar
  66. 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.CrossRefGoogle Scholar
  67. 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. 68.
    Maresca JA, Crowe SA, Macalady JL. Anaerobic photosynthetic ecosystems. Geobiology. 2012;10(3):193–5.CrossRefGoogle Scholar
  69. 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.CrossRefGoogle Scholar
  70. 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.CrossRefGoogle Scholar
  71. 71.
    Dietrich LEP, Tice MM, Newman DK. The co-evolution of life and Earth. Curr Biol. 2006;16(11):R395–400.CrossRefGoogle Scholar

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© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Research Department of Genetics, Evolution and EnvironmentUniversity College LondonLondonUK

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