Photosynthesis Research

, Volume 80, Issue 1–3, pp 373–386 | Cite as

Thinking About the Evolution of Photosynthesis

  • John M. Olson
  • Robert E. Blankenship
Article

Abstract

Photosynthesis is an ancient process on Earth. Chemical evidence and recent fossil finds indicate that cyanobacteria existed 2.5–2.6 billion years (Ga) ago, and these were certainly preceded by a variety of forms of anoxygenic photosynthetic bacteria. Carbon isotope data suggest autotrophic carbon fixation was taking place at least a billion years earlier. However, the nature of the earliest photosynthetic organisms is not well understood. The major elements of the photosynthetic apparatus are the reaction centers, antenna complexes, electron transfer complexes and carbon fixation machinery. These parts almost certainly have not had the same evolutionary history in all organisms, so that the photosynthetic apparatus is best viewed as a mosaic made up of a number of substructures each with its own unique evolutionary history. There are two schools of thought concerning the origin of reaction centers and photosynthesis. One school pictures the evolution of reaction centers beginning in the prebiotic phase while the other school sees reaction centers evolving later from cytochrome b in bacteria. Two models have been put forth for the subsequent evolution of reaction centers in proteobacteria, green filamentous (non-sulfur) bacteria, cyanobacteria, heliobacteria and green sulfur bacteria. In the selective loss model the most recent common ancestor of all subsequent photosynthetic systems is postulated to have contained both RC1 and RC2. The evolution of reaction centers in proteobacteria and green filamentous bacteria resulted from the loss of RC1, while the evolution of reaction centers in heliobacteria and green sulfur bacteria resulted from the loss of RC2. Both RC1 and RC2 were retained in the cyanobacteria. In the fusion model the most recent common ancestor is postulated to have given rise to two lines, one containing RC1 and the other containing RC2. The RC1 line gave rise to the reaction centers of heliobacteria and green sulfur bacteria, and the RC2 line led to the reaction centers of proteobacteria and green filamentous bacteria. The two reaction centers of cyanobacteria were the result of a genetic fusion of an organism containing RC1 and an organism containing RC2. The evolutionary histories of the various classes of antenna/light-harvesting complexes appear to be completely independent. The transition from anoxygenic to oxygenic photosynthesis took place when the cyanobacteria learned how to use water as an electron donor for carbon dioxide reduction. Before that time hydrogen peroxide may have served as a transitional donor, and before that, ferrous iron may have been the original source of reducing power.

Carl Bauer Chlorosomes Endosymbiosis FMO protein fusion model Granick hypothesis Radhey Gupta Hyman Hartman Wolfgang Junge Lynn Margulis Paul Mathis David Mauzerall Terrance Meyer microfossils Armin Mulkidjanian Wolfgang Nitschke Beverly Pierson Jason Raymond selective loss model stromatolites Wim Vermaas whole genome analysis Jin Xiong 

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References

  1. Awramik SM, Schopf JW and Walter MR (1983) Filamentous fossil bacteria 3.5×109 years old from the Archean of Western Australia. Precambrian Res 20: 357Google Scholar
  2. Bader KP (1994) Physiological and evolutionary aspects of the O2/H2O-cycle in cyanobacteria. Biochim Biophys Acta 1188: 213–219Google Scholar
  3. Baranov RA, Ananyev GM, Klimov VV and Dismukes GC (2000) Bicarbonate accelerates assembly of the inorganic core of the water-oxidizing complex in manganese-depleted Photosystem II: A proposed biogeochemical role for atmospheric carbon dioxide in oxygenic photosynthesis. Biochemistry 39: 6060–6065PubMedGoogle Scholar
  4. Benner SA (2002) The past as the key to the present. Resurrection of ancient proteins from eosinophils. Proc Natl Acad Sci USA 99: 4760–4761PubMedGoogle Scholar
  5. Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 51: 91–111Google Scholar
  6. Blankenship RE (2002) Molecular Mechanisms of Photosynthesis, Chapter 11. Blackwell Science, Malden, MassachusettsGoogle Scholar
  7. Blankenship RE and Hartman H (1998) The origin and evolution of oxygenic photosynthesis. TIBS 23: 94–97PubMedGoogle Scholar
  8. Blankenship RE and Matsuura K (2003) Antenna complexes from green photosynthetic bacteria. In: Green BR and Parsons WW (eds) Light-Harvesting Antennas, pp 195–217. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  9. Borda MJ, Elsetinow AR, Schooen MA and Strongin DR (2001) Pyrite-induced hydrogen peroxide formation as a driving force in the evolution of photosynthetic organisms on an early Earth. Astrobiology 1: 283–288PubMedGoogle Scholar
  10. Brasier MD, Green OR, Jephcoat AP, Kleppe AK, Van Kranendonk MJ, Lindsay JF, Steel A and Grassineau NV (2002) Questioning the evidence for Earth's oldest fossils. Nature 416: 76–81PubMedGoogle Scholar
  11. Bryant DA, Vassilieva EV, Frigaard N-U and Li H (2002) Selective protein extraction from Chlorobium tepidum chlorosomes using detergents. Evidence that CsmA forms multimers and binds bacteriochlorophyll a. Biochemistry 41: 14403–14411PubMedGoogle Scholar
  12. Buick R (2001) Life in the Archean. In: Briggs DEG and Crowther PR (eds) Paleobiology II, pp 13–21. Blackwell Science, OxfordGoogle Scholar
  13. 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: 7134–7138Google Scholar
  14. Catling D and Zahnle K (2002) Evolution of atmospheric oxygen.In: Holton J, Curry J and Pyle J (eds) Encyclopedia of Atmospheric Sciences, pp 754–761. Academic Press, New YorkGoogle Scholar
  15. Chisholm D and Williams JGK (1988) Nucleotide sequence of psbC, the gene encoding the CP-43 chlorophyll a-binding protein of Photosystem II, in the cyanobacterium Synechocystis 6803. Plant Mol Biol 10: 293–301Google Scholar
  16. 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. American Society of Microbiology, Washington, DCGoogle Scholar
  17. Dismukes GC (1996) Manganese enzymes with binuclear active sites. Chem Rev 96: 2909–2926PubMedGoogle Scholar
  18. Dismukes GC, Klimov VV, Baronov SV, Kozlov YN and DasGupta J and Tyryshkin A (2001) The origin of atmospheric oxygen on Earth: The innovation of oxygenic photosynthesis. Proc Natl Acad Sci USA 98: 2170–2175PubMedGoogle Scholar
  19. 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
  20. Granick S (1957) Speculations on the origins and evolution of photosynthesis. Ann N Y Acad Sci 69: 292–308PubMedGoogle Scholar
  21. Granick S (1965) Evolution of heme and chlorophyll. In: Bryson V and Vogel HJ (eds) Evolving Genes and Proteins, pp 67–88.Academic Press, New YorkGoogle Scholar
  22. Green BR (2003) The evolution of light-harvesting antennas. In: Green BR and Parsons WW (eds) Light-Harvesting Antennas, pp 129–168. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  23. Greenbaum E, Lee JW, Tevault CV, Blankinship SL and Mets LJ (1995) CO2 fixation and photoevolution of H2 and O2 in a mutant of Chlamydomonas lacking Photosystem I. Nature 376: 438–441Google Scholar
  24. Greenbaum E, Lee JW, Tevault CV, Blankinship SL and Mets LJ (1997) Correction: CO2 fixation and photoevolution of H2 and O2 in a mutant of Chlamydomonas lacking Photosystem I. Nature 388: 808Google Scholar
  25. Grossman AR, Bhaya D, Apt KE and Kehoe DM (1995) Light harvesting complexes in oxygenic photosynthesis. Diversity, control and evolution. Ann Rev Genet 29: 231–288PubMedGoogle Scholar
  26. Gupta RS (2003) Evolutionary relationships among photosynthetic bacteria. Photosynth Res 76: 173–183PubMedGoogle Scholar
  27. Han T-M and Runnegar B (1992) Megascopic eukaryotic algae from the 2.1 billion-year-old Negaunee iron formation, Michigan. Science 257: 232–235PubMedGoogle Scholar
  28. Hartman H (1998) Photosynthesis and the origin of life. Origins Life Evol Biosphere 28: 515–521Google Scholar
  29. Heathcote P, Fyfe PK and Jones MR (2002) Reaction centres: the structure and evolution of biological solar power. TIBS 27: 79–87PubMedGoogle Scholar
  30. Heising S and Schink B (1998) Phototrophic oxidation of ferrous iron by a Rhodomicrobium vannieli strain. Microbiology 144: 2263–2269PubMedGoogle Scholar
  31. 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: 116–124Google Scholar
  32. Hofmann HJ and Schopf JW (1983) Early proterozoic microfossils. In: Schopf JW (ed) Earth's Earliest Biosphere, pp 321–360. Princeton University Press, Princeton, New JerseyGoogle Scholar
  33. Kastings 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
  34. Kazmierczak J and Altermann W (2002) Neoarchean biomineralization by benthic cyanobacteria. Science 298: 2351PubMedGoogle Scholar
  35. Kazmierczak J and Kremer B (2002) Thermal alteration of the Earth's oldest fossils. Nature 420: 477–478PubMedGoogle Scholar
  36. Kikuchi H, Wako H, Yura K, Go M and Mimuro M (2000) Significance of a two-domain structure in subunits of phycobiliproteins revealed by the normal mode analysis. Biophys J 79: 1587–1600PubMedGoogle Scholar
  37. Knoll A (1992) The early evolution of eukaryotes: a geological perspective. Science 256: 622–627PubMedGoogle Scholar
  38. LaRoche J, van der Staay GWM, Partensky F, Ducret A, Aebersold R, Li R, Golden SS, Hiller RG, Wrench PM, Larkum AWD and Green BR (1996) Independent evolution of the prochlorophyte and green plant chlorophyll a/b light-harvesting proteins. Proc Natl Acad Sci USA 93: 15244–15248Google Scholar
  39. Li Y-F, Zhou W, Blankenship RE and Allen JP (1997) Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum. J Mol Biol 272: 1–16Google Scholar
  40. Loach PA and Parkes-Loach PS (1995) Structure-function relationships in core light-harvesting complexes (LH1) as determined by characterization of the structural subunit and by reconstitution experiments. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 437–471. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  41. 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: 1930–1934PubMedGoogle Scholar
  42. 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
  43. Margulis L (1970) Origin of Eukaryotic Cells. Yale University Press, New Haven, ConnecticutGoogle Scholar
  44. Mathis P (1990) Compared structure of plant and bacterial photosynthetic reaction centers. Evolutionary implications. Biochim Biophys Acta 1018: 163–167Google Scholar
  45. Matthews BW, Fenna RE, Bolognesi MC, Schmid MF and Olson JM (1979) Structure of a bacteriochlorophyll a-protein from the green photosynthetic bacterium Prosthecochloris aestuarii.J Mol Biol 131: 259–285PubMedGoogle Scholar
  46. 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
  47. Mauzerall D (1978) Bacteriochlorophyll and photosynthetic evolution.In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 223–231. Plenum Press, New YorkGoogle Scholar
  48. Mauzerall D (1992) Light, iron, Sam Granick and the origin of life. Photosynth Res 33: 163–170Google Scholar
  49. McKay CP and Hartman H (1991) Hydrogen peroxide and the evolution of oxygenic photosynthesis. Origins Life Evol Biosphere 21: 157–163Google Scholar
  50. Mercer-Smith JA and Mauzerall D (1984) Photochemistry of porphyrins: a model for the origin of photosynthesis. Photochem Photobiol 39: 397–405PubMedGoogle Scholar
  51. Meyer TE (1994) Evolution of photosynthetic reaction centers and light harvesting chlorophyll proteins. BioSystems 33: 167–175PubMedGoogle Scholar
  52. 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
  53. Michel H and Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of Photosystem II. Biochemistry 27: 1–7Google Scholar
  54. Mojzsis SJ, Arrhenius G, McKeegan KD, Harrison TM, Nutman AP and Friend CRL (1996) Evidence for life on Earth before 3800 million years ago. Nature 384: 55–59PubMedGoogle Scholar
  55. Montaño GA, Wu H-M, Lin S, Brune DC and Blankenship RE (2003) Isolation and characterization of the B798 lightharvesting baseplate from the chlorosomes of Chloroflexus aurantiacus.Biochemistry 42: 10246–10251PubMedGoogle Scholar
  56. Mulkidjanian AY and Junge W (1997) On the origin of photosynthesis as inferred from sequence analysis. Photosynth Res 51: 27–42Google Scholar
  57. Nitschke W and Rutherford AW (1991) Photosynthetic reaction centres — variations on a common structural theme. TIBS 16: 241–245PubMedGoogle Scholar
  58. 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
  59. Olson JM (1970) Evolution of photosynthesis. Science 168: 438–446PubMedGoogle Scholar
  60. Olson JM (1978) Precambrian evolution of photosynthetic and respiratory organisms. Evol Biol 11: 1–37Google Scholar
  61. Olson JM (1981) Evolution of photosynthetic reaction centers. BioSystems 14: 89–94PubMedGoogle Scholar
  62. Olson JM (1998) Chlorophyll organization and function in green photosynthetic bacteria. Photochem Photobiol 67: 61–75Google Scholar
  63. Olson JM (1999) Early evolution of chlorophyll-based photosystems. Chemtracts Biochem Mol Biol 12: 468–482Google Scholar
  64. Olson JM (2001) 'Evolution of Photosynthesis' (1970), reexamined thirty years later. Photosynth Res 68: 95–112PubMedGoogle Scholar
  65. Olson JM and Pierson BK (1986) Photosynthesis 3.5 thousand million years ago. Photosynth Res 9: 251–259Google Scholar
  66. Olson JM and Pierson BK (1987a) Evolution of reaction centers in photosynthetic prokaryotes. Ann Rev Cytol 108: 209–248Google Scholar
  67. Olson JM and Pierson BK (1987b) Origin and evolution of photosynthetic reaction centers. Orig Life 17: 419–430Google Scholar
  68. Olson JM and Raymond J (2003) The FMO protein is related to PscA in the reaction center of green sulfur bacteria. Photosynth Res 75: 277–285PubMedGoogle Scholar
  69. Olson JM, Prince RC and Brune DC (1976) Reaction center complexes from green bacteria. In: Chlorophyll Proteins, Reaction Centers and Photosynthetic Membranes, Vol. 28, Brookhaven Symposia in Biology, pp 238–246. Brookhaven National Laboratory, Upton, New YorkGoogle Scholar
  70. Palmer JD and Delwich CE (1996) Second hand chloroplasts and the case of the disappearing nucleus. Proc Natl Acad Sci 93: 7432–7435PubMedGoogle Scholar
  71. Pasteris JD and Wopenka B (2002) Images of the Earth's earliest fossils? Nature 420: 476–477PubMedGoogle Scholar
  72. 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: 21901–21908PubMedGoogle Scholar
  73. Pierson BK and Olson JM (1989) Evolution of photosynthesis in anoxygenic photosynthetic procaryotes. In: Cohen Y and Rosenberg E (eds) Microbial Mats, Physiological Ecology of Benthic Communities, pp 402–427. American Society of Microbiology, Washington, DCGoogle Scholar
  74. 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: 585–589PubMedGoogle Scholar
  75. Rasmussen B (2000) Filamentous microfossils in a 3235-millionyear-old volcanogenic massive sulphide deposit. Nature 405: 676–679PubMedGoogle Scholar
  76. Raymond J, Zhaxybayeva O, Gogarten JP, Gerdes SY and Blankenship RE (2002) Whole-genome analysis of photosynthetic prokaryotes. Science 298: 1616–1620PubMedGoogle Scholar
  77. Raymond J, Siefert J, Staples C and Blankenship RE (2003a) The natural history of nitrogen fixation. Mol Biol Evol (in press)Google Scholar
  78. Raymond J, Zhaxybayeva O, Gogarten JP and Blankenship RE (2003b) Evolution of photosynthetic prokaryotes: a maximum likelihood mapping approach. Phil Trans R Soc B 358: 223–230PubMedGoogle Scholar
  79. Robert B and Moenne-Loccoz P (1989) FrUn site possible pour d l'accepteur primaire d'electrons du Photosystème 1. C R Acad Sci Paris SerieIII 308: 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. Rutherford AW and Nitschke W (1996) In: Baltscheffsky H (ed) Origin and Evolution of Biological Energy Conversion, pp 143–175. VCH Publishers, New YorkGoogle Scholar
  82. Samuilov VD (1997) Photosynthetic oxygen: the role of H2O2: a review. Biochemistry (Moscow) 62: 451–454Google Scholar
  83. Schidlowski M (1988) A 3800-million-year isotopic record of life from carbon in sedimentary rocks. Nature 333: 313–318Google Scholar
  84. Schidlowski M, Hayes JMand Kaplan IR (1983) Isotopic inferences of ancient biochemistries: carbon, sulfur, hydrogen and nitrogen. In: Schopf JW (ed) Earth's Earliest Biosphere, pp 149–185. Princton University Press, Princeton, New JerseyGoogle Scholar
  85. Schirmer T, Bode W, Huber R, Sidler W and Zuber H (1985) Xray crystallographic structure of the light-harvesting biliprotein c-phycocyanin from the thermophilic cyanobacterium Mastigocladus laminosus and its resemblance to globin structures. J Mol Biol 184: 257–277PubMedGoogle Scholar
  86. Schopf JW (1968) Microflora of the Bitter Springs Formation, Late Precambrian, Central Australia. J Paleontol 42: 651–688Google Scholar
  87. Schopf JW (1974) Paleobiology of the Precambrian: The age of blue-green algae. Evol Biol 7: 1–38Google Scholar
  88. Schopf JW (1993) Microfossils of the early Archean Apex chert: New evidence of the antiquity of life. Science 260: 640–646PubMedGoogle Scholar
  89. Schopf JW and Barghoorn ES (1967) Alga-like fossils from the early Precambrian of South Africa. Science 156: 508–512Google Scholar
  90. Schopf JW and Blacic JM (1971) New microorganisms from the Bitter Springs Formation (Late Precambrian) of the north-central Amadeus Basin, Australia. J Paleontol 45: 925–960Google Scholar
  91. Schopf JW and Packer BM (1987) Early Archean (3.3-billion to 3.5-billion-year-old) microfossils from Warrawoona Group, Australia. Science 273: 70–73Google Scholar
  92. 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
  93. Schopf JW, Kudryavtsev AB, Agresti DG, Wdowiak TJ and Czaja AD (2002) Reply to Images of the Earth's earliest fossils. Nature 420: 477Google Scholar
  94. 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: 297–314PubMedGoogle Scholar
  95. 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: 663–676PubMedGoogle Scholar
  96. Summons RE, Jahnke LL, Hope JM and Logan GA (1999) 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400: 554–557PubMedGoogle Scholar
  97. Vermaas WFJ (1994) Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosynth Res 41: 285–294PubMedGoogle Scholar
  98. Vermaas WFJ (2002) Evolution of photosynthesis. In:Encyclopedia of Life Sciences, pp 1–18. Nature Publishing Group, London (http://www.els.net)Google Scholar
  99. Vermaas WFJ, Williams JGK and Arntzen CJ (1987) Sequencing and modification of psbB, the gene encoding the CP-47 protein of Photosystem II, in the cyanobacterium Synechocystis 6803. Plant Mol Biol 8: 317–326Google Scholar
  100. Walker JCG (1983) Possible limits on the composition of the Archaean ocean. Nature 302: 518–520Google Scholar
  101. Walter MR (1983) Archean stromatolites: evidence of the Earth's earliest benthos. In: Schopf JW (ed) Earth's Earliest Biosphere, pp 187–213. Princeton University Press, Princeton, New JerseyGoogle Scholar
  102. Widdel F, Schnell S, Heising S, Ehrenreich A, Assmus B and Schink B (1993) Ferrous iron oxidation by anoxygenic phototrophic bacteria. Nature 362: 834–836Google Scholar
  103. Xiong J and Bauer CE (2002a) A cytochrome b origin of photosynthesic reaction centers: an evolutionary link between respiration and photosynthesis. J Mol Biol 322: 1025–1037PubMedGoogle Scholar
  104. Xiong J and Bauer CE (2002b) Complex evolution of photosynthesis. Annu Rev Plant Biol 53: 503–521PubMedGoogle Scholar
  105. 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: 14851–14856PubMedGoogle Scholar
  106. Xiong J, Fischer WM, Inoue K, Nakahara M and Bauer CE (2000) Molecular evidence for the early evolution of photosynthesis.Science 289: 1724–1730PubMedGoogle Scholar
  107. Yanyushin M (2002) Fractionation of cytochromes of phototrophically grown Chloroflexus aurantiacus. Is there a cytochrome bc complex among them? FEBS Lett 512: 125–128PubMedGoogle Scholar
  108. Zuber H and Brunisholz R (1991) Structure and function of antenna polypeptides and chlorophyll-protein complexes: Principles and variability. In: Scheer H (ed) Chlorophylls, pp 627–703. CRC, Boca Raton, FloridaGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2004

Authors and Affiliations

  • John M. Olson
    • 1
  • Robert E. Blankenship
    • 2
  1. 1.Department of Biochemistry and Molecular Biology, Lederle Graduate Research CenterUniversity of MassachusettsAmherstUSA
  2. 2.Department of Chemistry and BiochemistryArizona State UniversityTempeUSA

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