Photosynthesis Research

, Volume 68, Issue 2, pp 95–112

‘Evolution of Photosynthesis’ (1970), re-examined thirty years later

  • John M. Olson


I have re-examined my 1970 article ‘Evolution of Photosynthesis’ (Olson JM, Science 168: 438–446) to see whether any of my original proposals still survive. My original conviction that the evolution of photosynthesis was intimately connected with the origin of life has been replaced with the realization that photosynthesis may have been invented by the Bacteria after their divergence from the Archea. The common ancestor of all extant photosynthetic bacteria and cyanobacteria probably contained bacteriochlorophyll a, rather than chlorophyll a as originally proposed, and may have carried out CO2 fixation instead of photoassimilation. The first electron donors were probably reduced sulfur compounds and later ferrous iron. The common ancestor of all extant reaction centers was probably similar to the homodimeric RC1 of present-day green sulfur bacteria (Chlorobiaceae) and heliobacteria. In the common ancestor of proteobacteria and cyanobacteria, the gene for the primordial RC1 was apparently duplicated and one copy split into two genes, one for RC2 and the other for a chlorophyll protein similar to CP43 and CP47 in extant cyanobacteria and chloroplasts. Homodimeric RC1 and homodimeric RC2 functioned in series as in the Z-scheme to deliver electrons from Fe(OH)+ to NADP+, while RC1 and/or RC2 separately drove cyclic electron flow for the production of ATP. In the line of evolution leading to proteobacteria, RC1 and the chlorophyll protein were lost, but RC2 was retained and became heterodimeric. In the line leading to cyanobacteria, both RC1 and RC2 replaced bacteriochlorophyll a with chlorophyll a and became heterodimeric. Heterodimeric RC2 further coevolved with a Mn-containing complex to utilize water as the electron donor for CO2 fixation. The chlorophyll–protein was also retained and evolved into CP43 and CP47. Heliobacteria are the nearest photosynthetic relatives of cyanobacteria. The branching order of photosynthetic genes appears to be (1) proteobacteria, (2) green bacteria (Chlorobiaceae plus Chloroflexaceae), and (3) heliobacteria plus cyanobacteria.

chlorophyll synthesis common ancestor cyanobacteria cytochrome b electron donors for CO2 fixation evolution of photosynthesis green bacteria heliobacteria proteobacteria reaction center 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen TP, Feher G, Yeates TO, Komiya H and Rees DC (1987a) Structure of the reaction center from Rhodobacter sphaeroides R-26: The cofactors. Proc Natl Acad Sci USA 84: 5730–5734PubMedCrossRefGoogle Scholar
  2. Allen TP, Feher G, Yeates TO, Komiya H and Rees DC (1987b) Structure of the reaction center from Rhodobacter sphaeroides R-26: The protein subunits. Proc Natl Acad Sci USA 84: 6162–6166PubMedCrossRefGoogle Scholar
  3. Bader KP (1994) Physiological and evolutionary aspects of the O2/H2O-cycle in cyanobacteria. Biochim Biophys Acta 1188: 213–219CrossRefGoogle Scholar
  4. Barghoorn ES and Schopf JW (1966) Microorganisms three billion years old from the Precambrian of South Africa. Science 152: 758PubMedGoogle Scholar
  5. Beanland TJ (1990) Evolutionary relationships between ‘Q-type’ photosynthetic reaction centres: Hypothesis-testing using parsimony. J Theor Biol 145: 535–545PubMedCrossRefGoogle Scholar
  6. Berkner LV and Marshall LC (1965a) History of major atmospheric components. Proc Natl Acad Sci USA 53: 1215–1225CrossRefGoogle Scholar
  7. Berkner LV and Marshall LC (1965b) On the origin and rise of oxygen concentration in the Earth's atmosphere. J Atmos Sci 22: 225–261CrossRefGoogle Scholar
  8. Berkner LV and Marshall LC (1969) The rise and stability of the earth's atmosphere. In: Brookhaven Natl Lab Lect Sci Vistas Res, Vol 4, pp 113–122. Gordon and Breach, New YorkGoogle Scholar
  9. Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 51: 91–111CrossRefGoogle Scholar
  10. Blankenship RE and Hartman H (1998) The origin and evolution of oxygenic photosynthesis. TIBS 23: 94–97PubMedGoogle Scholar
  11. Bogorad L (1965) Chlorophyll biosynthesis. In: Goodwin TW (ed) Chemistry and Biochemistry of Plant Pigments, p 64. Academic Press, LondonGoogle Scholar
  12. Brockmann H and Lipinski A (1983) Bacteriochlorophyll g. A new bacteriochlorophyll from Heliobacterium chlorum. Arch Microbiol 136: 17–19CrossRefGoogle Scholar
  13. Bryant DA (1992) Molecular biology of Photosystem I. In: Barber J (ed) The Photosystems: Structure, Function and Molecular Biology, pp 501–549. Elsevier Science Publishers, AmsterdamGoogle Scholar
  14. Buick R (1992) The antiquity of oxygenic photosynthesis: Evidence from stromatolites in sulphate-deficient Archean lakes. Science 255: 74–77PubMedGoogle Scholar
  15. Burke DH, Hearst JE and Sidow A (1993) Early evolution of photosynthesis: Clues from nitrogenase and chlorophyll iron proteins. Proc Natl Acad Sci USA 93: 7134–7138CrossRefGoogle Scholar
  16. Canfield DE, Habicht KS and Thamdrup B (2000) The Archean sulfur cycle and the early history of atmospheric oxygen. Science 288: 658–661PubMedCrossRefGoogle Scholar
  17. Cloud Jr PE (1965a) Chairman's summary remarks. Proc Natl Acad Sci USA 53: 1169–1172CrossRefGoogle Scholar
  18. Cloud Jr PE (1965b) Significance of the Gunflint (Precambrian) microflora. Science 148: 27–35PubMedGoogle Scholar
  19. Cohen Y (1984) Oxygenic photosynthesis, anoxygenic photosynthesis and sulfate reduction in cyanobacterial mats. In: Klug MJ and Reddy CA (eds) Current Perspectives in Microbial Ecology, pp 435–441. Am Society of Microbiology, Washington, DCGoogle Scholar
  20. Deisenhofer J, Epp O, Sinning I and Michel H (1995) Crystallographic refinement at 2.3 Å resolution and refined model of the photosynthetic reaction centre from Rhodopseudomonas viridis. J Mol Biol 246: 429–457.PubMedCrossRefGoogle Scholar
  21. Dismukes GC (1996) Manganese enzymes with binuclear active sites. Chem Rev 96: 2909–2926PubMedCrossRefGoogle Scholar
  22. Eglinton G and Calvin M (1967) Chemical fossils. Sci Am 216: 32–43CrossRefGoogle Scholar
  23. Ehrenreich A and Widdel F (1994) Anaerobic oxidation of ferrous iron by purple bacteria, a new type of phototrophic metabolism. Appl Environ Microbiol 4: 4517–4526Google Scholar
  24. Engel AEJ, Nagy B, Nagy LA, Engel CG, Kremp GOW and Drew CM (1968) Alga-like forms in Onverwacht Series, South Africa: Oldest recognized lifelike forms on Earth. Science 161: 1005–1008PubMedGoogle Scholar
  25. Feiler U and Hauska G (1995) The reaction center from green sulfur bacteria. In Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 665–685. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  26. Harold FM (1986) The Vital Force: A Study of Bioenergetics, Freeman, New York, p 120Google Scholar
  27. Hartman H (1998) Photosynthesis and the origin of life. Origins Life Evol Biosphere 28: 515–521CrossRefGoogle Scholar
  28. Heath RL (1971) Hydrazine as an electron donor to the wateroxidation site in photosynthesis. Biochim Biophys Acta 245: 160–164PubMedCrossRefGoogle Scholar
  29. Heising S and Schink B (1998) Phototrophic oxidation of ferrous iron by a Rhodomicrobium vannieli strain. Microbiology 144: 2263–2269PubMedCrossRefGoogle Scholar
  30. Heising S, Richter L, Ludwig W and Schink B (1999) Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a 'Geospirillum' sp. strain. Arch Microbiol 172: 116–124PubMedCrossRefGoogle Scholar
  31. Holland HD (1994) Early Proterozoic atmosphere change. In: Bengtson S (ed) Early Life on Earth, pp 237–244. Columbia University Press, New YorkGoogle Scholar
  32. Holland HD, Lazar B and McCaffrey M (1986) Evolution of the atmosphere and oceans. Nature 320: 33–37Google Scholar
  33. Holmes A (1954) The oldest dated minerals of the Rhodesian Shield. Nature 173: 612–614CrossRefGoogle Scholar
  34. Izawa S, Heath RL and Hind G (1969) The role of chloride in photosynthesis: III. The effect of artificial electron donors upon electron transport. Biochim Biophys Acta 180: 388PubMedCrossRefGoogle Scholar
  35. Johansen J (1988) A possible role for hydrogen peroxide as a naturally occurring electron donor in photosynthetic oxygen evolution. Biochem Biophys Acta 933: 406–412CrossRefGoogle Scholar
  36. Kasting JF (1993) Earth's early atmosphere. Science 259: 920–926PubMedGoogle Scholar
  37. Kasting JF and Brown LL (1998) The early atmosphere as a source of biogenic compounds. In: Brack A (ed) The Molecular Origins of Life: Assembling the Pieces of the Puzzle, pp 35–56. Cambridge University Press, Cambridge, UKGoogle Scholar
  38. Kasting JF, Pollack JB and Crisp D (1984) Effects of high CO2 levels on surface temperature and atmospheric oxidation state of the early Earth. J Atmos Chem 1: 403–428PubMedCrossRefGoogle Scholar
  39. Kobayashi M, Oh-oka H, Akutsu S, Akiyama M, Tominaga K, Kise H, Nishida F, Watanabe T, Amesz J, Koizumi M, Ishida N and Kano H (2000) The primary electron acceptor of green sulfur bacteria, bacteriochlorophyll 663, is chlorophyll a esterified with 2,6-phytadienol. Photosynth Res 63: 269–280PubMedCrossRefGoogle Scholar
  40. Nagashima KVP, Hanada S, Hiraishi A, Shimada K and Matsuura K (1995) Phylogenetic analysis of photosynthetic reaction centers of purple bacteria and green filamentous bacteria. In: Matis P (ed) Photosynthesis: From Light to Biosphere, Vol I, pp 975–978. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  41. Nagashima KVP, Hiraishi A, Shimada K and Matsuura K (1997) Horizontal transfer of genes coding for the photosynthetic reaction centers of purple bacteria. J Mol Evol 45: 131–136PubMedCrossRefGoogle Scholar
  42. Knox RS (1969) Thermodynamics and the primary processes of photosynthesis. Biophys J 9: 1351PubMedGoogle Scholar
  43. Laselles J (1968) The bacterial photosynthetic apparatus. Adv Microbiol Physiol 2: 1–42Google Scholar
  44. Latimer WM(1952) The Oxidation States of the Elements and Their Potentials in Aqueous Solution. Prentice-Hall, New YorkGoogle Scholar
  45. Lockhart PJ, Larkum AWD, Steel MA, Waddell PJ and Penny D (1996) Evolution of chlorophyll and bacteriochlorophyll: The problem of invariant sites in sequence analysis. Proc Natl Acad Sci USA 93: 1930–1934PubMedCrossRefGoogle Scholar
  46. Margulies MM (1991) Sequence similarity between Photosystems I and II. Identification of a Photosystem I reaction center transmembrane helix that is similar to transmembrane helix IV of the D2 subunit of Photosystem II and theMsubunit of the non-sulfur and flexible green bacteria. Photosynth Res 29: 133–147Google Scholar
  47. Mathis P (1990) Compared structure of plant and bacterial photosynthetic reaction centers. Evolutionary implications. Biochim Biophys Acta 1018: 163–167CrossRefGoogle Scholar
  48. Mauzerall D (1977) Porphyrins, chlorophyll, and photosynthesis. In: Trebst A and Avron M (eds) Encyclopedia of Plant Physiology New Series, Vol 5, pp 117–124. Springer-Verlag, BerlinGoogle Scholar
  49. Mauzerall D (1992) Light, iron, Sam Granick and the origin of life. Photosynth Res 33: 163–170CrossRefGoogle Scholar
  50. McKay CP and Hartman H (1991) Hydrogen peroxide and the evolution of oxygenic photosynthesis. Origins Life Evol Biosphere 21: 157–163CrossRefGoogle Scholar
  51. Mercer-Smith JA and Mauzerall D (1984) Photochemistry of porphyrins: A model for the origin of photosynthesis. Photochem Photobiol 39: 397–405PubMedGoogle Scholar
  52. Meyer TE (1994) Evolution of photosynthetic reaction centers and light harvesting chlorophyll proteins. BioSystems 33: 167–175PubMedCrossRefGoogle Scholar
  53. Meyer TE, Van Beeumen JJ, Ambler RP and Cusanovich MA (1996) The evolution of electron transfer proteins in photosynthetic bacteria and denitrifying pseudomonads. In: Baltscheffsky H (ed) Origin and Evolution of Biological Energy Conversion, pp 71–108. VCH Publishers, New YorkGoogle Scholar
  54. Morell V (1997) Microbiology's scarred revolutionary. Science 276: 699–702PubMedCrossRefGoogle Scholar
  55. Mulkidjanian AY and Junge W (1997) On the origin of photosynthesis as inferred from sequence analysis. Photosynth Res 51: 27–42CrossRefGoogle Scholar
  56. Nitschke W, Kramer DM, Riedel A and Liebl U (1995) From naphtho-to benzoquinones — (R)evolutionary reorganizations of electron transfer chains. In: Matis P (ed) Photosynthesis: From Light to Biosphere, Vol I, pp 945–948. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  57. Nitschke W, Mühlenhoff U and Liebl U (1998) Evolution. In: Raghavendra A (ed) Photosynthesis: A Comprehensive Treatise, pp 285–304. Cambridge University Press, Cambridge, UKGoogle Scholar
  58. Ochman H, Lawence JG and Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405: 299–304PubMedCrossRefGoogle Scholar
  59. Ohmoto H, Kakegawa T and Lowe DR (1993) 3.4 billion-year-old biogenic pyrites from Barberton, South Africa: Sulfur isotope evidence. Science 262: 555–557PubMedGoogle Scholar
  60. Olson JM (1970) Evolution of photosynthesis. Science 168: 438–446PubMedGoogle Scholar
  61. Olson JM (1978) Precambrian evolution of photosynthetic and respiratory organisms. Evol Biol 11: 1–37Google Scholar
  62. Olson JM (1981a) Evolution of photosynthetic and respiratory prokaryotes and organelles. Ann N Y Acad Sci 361: 8–19PubMedGoogle Scholar
  63. Olson JM (1981b) Evolution of photosynthetic reaction centers. Biosystems 14: 89–94PubMedCrossRefGoogle Scholar
  64. Olson JM (1996) Iron—sulfur-type reaction centers: Introduction. Photochem Photobiol 64: 1–4Google Scholar
  65. Olson JM (1999) Early evolution of chlorophyll-based photosystems. Chemtracts—Biochemistry and Molecular Biology 12: 468–482Google Scholar
  66. Olson JM and Pierson BK (1986) Photosynthesis 3.5 thousand million years ago. Photosynth Res 9: 251–259CrossRefGoogle Scholar
  67. Olson JM and Pierson BK (1987a) Evolution of reaction centers in photosynthetic prokaryotes. Ann Rev Cytol 108: 209–248CrossRefGoogle Scholar
  68. Olson JM and Pierson BK (1987b) Origin and evolution of photosynthetic reaction centers. Orig Life 17: 419–430CrossRefGoogle Scholar
  69. Oparin AI (1968) Genesis and Evolutionary Development of Life. Academic Press, New YorkGoogle Scholar
  70. Pace NR (1997) A molecular view of microbial diversity and the biosphere. Science 276: 734–740PubMedCrossRefGoogle Scholar
  71. Pierre Y, Breyton C, Lemoine Y, Robert B, Vernotte C and Popot JL (1997) On the presence and role of chlorophyll a in the cytochrome b 6 f complex. J Biol Chem 272: 21901–21908PubMedCrossRefGoogle Scholar
  72. Pierson BK (1994) The emergence, diversification and role of photosynthetic eubacteria. In: Bengtson S (ed) Early Life on Earth, pp 161–180. Columbia University Press, New YorkGoogle Scholar
  73. Pierson BK and Olson JM (1987) Photosynthetic bacteria. In: Amesz J (ed) Photosynthesis, pp 21–42. Elsevier Science Publishers, AmsterdamGoogle Scholar
  74. Pierson BK and Olson JM(1989) Evolution of photosynthesis in anoxygenic photosynthetic procaryoytes. In: Cohen Y and Rosenberg E (eds) Microbial Mats, Physiological Ecology of Benthic Communities, pp 402–427. American Society of Microbiology, Washington, DCGoogle Scholar
  75. Pierson BK and Thornber JP (1983) Isolation and spectral characterization of photochemical reaction centers from the thermophilic green bacterium Chloroflexus aurantiacus strain J-10-f1. Proc Natl Acad Sci USA 80: 80–84PubMedCrossRefGoogle Scholar
  76. Pierson BK, Parenteau MN and Griffin BM (1999) Phototrophs in high-iron-concentration microbial mats: Physiological ecology of phototrophs in an iron-depositing hot spring. Appl Environ Microbiol 65: 5474–5483PubMedGoogle Scholar
  77. Poggese C, De Laureto PP, Giacometti GM, Rigoni F and Barbato R (1997) Cytochrome b 6/f complex from the cyanobacterium Synochocystis 6803: Evidence of dimeric organization and identification of chlorophyll-binding subunit. FEBS Lett 414: 585–589PubMedCrossRefGoogle Scholar
  78. Ponnamperuma C (1968) Ultraviolet radiation and the origin of life. Photophysiology 3: 253–267Google Scholar
  79. Robert B and Moenne-Loccoz P (1989) Un site possible pour d l'accepteur primaire d'electrons du photosystème 1. C R Acad Sci Paris 308 Serie III: 407–409Google Scholar
  80. Robert B and Moenne-Loccoz P (1990) Is there a proteic substructure common to all photosynthetic reaction centers? In: Balscheffsky M (ed) Current Research in Photosynthesis, Vol 1, pp 65–68. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  81. Ross RT and Calvin M (1967) Thermodynamics of light emission and free energy storage in photosynthesis. Biophys J 7: 595–614PubMedCrossRefGoogle Scholar
  82. Samuilov VD (1997) Photosynthetic oxygen: the role of H2O2. A review. Biochemistry (Moscow) 62: 451–454Google Scholar
  83. Schopf JW and Barghoorn ES (1967) Alga-like fossils from the Early Precambrian of South Africa. Science 156: 508–512PubMedGoogle Scholar
  84. Schopf JW and Walter MR (1983) Archean microfossils: New evidence of ancient microbes. In: Schopf JW (ed) Earth's Earliest Biosphere, pp 214–239. Princeton University Press, Princeton, New JerseyGoogle Scholar
  85. Schubert WD, Klukas O, Saenger W, Witt HT, Fromme P and Krauss N (1998) A common ancestor for oxygenic and anoxygenic photosynthetic systems: A comparison based on the structural model of Photosystem I. J Mol Biol 280: 297–314PubMedCrossRefGoogle Scholar
  86. Schütz M, Brugna M, Lebrun E, Baymann F, Huber R, Stetter K-O, Hauska G, Toci R, Lemesle-Meunier D, Tron P, Schmidt C and Nitschke W(2000) Early evolution of cytochrome bc-complexes. J Mol Biol 300: 663–676PubMedCrossRefGoogle Scholar
  87. Stryer L (1988) Biochemistry, 3rd edition. Freeman, New York, p 411Google Scholar
  88. Towe KM (1994) Earth's early atmosphere: Constraints and opportunities for early evolution. In: Bengtson S (ed) Early Life on Earth, pp 36–47. Columbia University Press, New YorkGoogle Scholar
  89. Van De Meent EJ, Kobayashi M, Erkelens C, Van Veelen PA, Otte SCM, Inoue K, Wanatabe T and Amesz J (1992) The nature of the primary electron acceptor in green sulfur bacteria. Biochim Biophys Acta 1102: 371–378CrossRefGoogle Scholar
  90. Vermaas WFJ (1994) Evolution of heliobacteria: Implications for photosynthetic reaction center complexes. Photosynth Res 41: 285–294PubMedCrossRefGoogle Scholar
  91. Vogel HJ and Vogel RH (1967) Some chemical glimpses of evolution. Chem Eng News 45: 90–97Google Scholar
  92. Walker JCG (1983) Possible limits on the composition of the Archaean ocean. Nature 302: 518–520CrossRefGoogle Scholar
  93. Walker JCG, Klein C, Schidlowski M, Schopf JW, Stevenson DJ and Walter MR (1983) Environmental evolution of the Archean-Early Proterozoic Earth. In: Schopf JW (ed) Earth's Earliest Biosphere, pp 260–290. Princeton University Press, Princeton, New JerseyGoogle Scholar
  94. Widdel F, Schnell S, Heising S, Ehrenreich A, Assmus B and Schink B (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362: 834–836CrossRefGoogle Scholar
  95. Woese CR (1987) Bacterial evolution. Microbiol Rev 51: 221–271PubMedGoogle Scholar
  96. Wilson CL, Hinman NW and Sheridan RP (2000a) Hydrogen peroxide formation and decay in iron-rich geothermal waters: The relative roles of abiotic and biotic mechanisms. Photochem Photobiol 71: 691–699PubMedCrossRefGoogle Scholar
  97. Wilson CL, Hinman NW, Cooper WJ and Brown CF (2000b) Hydrogen peroxide cycling in surface geothermal waters of Yellowstone National Park. Environ Sci Technol 34: 2655–2662CrossRefGoogle Scholar
  98. Xiong J, Inoue K and Bauer CE (1998) Tracking molecular evolution of photosynthesis by characterization of a major photosynthesis gene cluster from Heliobacillus mobilis. Proc Natl Acad Sci USA 95: 14851–14856PubMedCrossRefGoogle Scholar
  99. Xiong J, Fischer WM, Inoue K, Nakahara M and Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis. Science 289: 1724–1730PubMedCrossRefGoogle Scholar
  100. Yachandra VK, Sauer K and Klein MP (1996) Manganese cluster in photosynthesis: Where plants oxidize water to dioxygen. Chem Rev 96: 2927–2950PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • John M. Olson
    • 1
  1. 1.Department of Biochemistry and Molecular Biology, Lederle Graduate Research CenterUniversity of MassachusettsAmherstUSA

Personalised recommendations