Advertisement

Photosynthesis Research

, Volume 35, Issue 1, pp 87–96 | Cite as

History of concepts of the comparative biochemistry of oxygenic and anoxygenic photosyntheses

  • Howard Gest
Regular Paper

Abstract

Experiments of Hans Molisch in 1907 demonstrated that purple bacteria do not evolve molecular oxygen during photosynthetic metabolism, and can use organic compounds as sources of cell carbon for anaerobic ‘photoheterotrophic’ growth. Molisch's conclusion that he discovered a new photosynthetic growth mode was not accepted for some 30 years because of the prevailing definition of photosynthesis as light-dependent conversion of carbon dioxide and inorganic reductants to cell materials. Meanwhile, during the decade of the 1930s, Cornelis van Niel formulated the ‘comparative biochemical watercleavage hypothesis’ of photosynthesis, which enjoyed great popularity for about 20 years. According to this concept, photolysis of water yielded ‘H’ and ‘OH’, the former acting as the hydrogen donor for CO2 reduction in all modes of photosynthesis. Oxygenic organisms were presumed to contain a unique biochemical system capable of converting ‘OH’ to water and O2. To explain the absence of O2 formation by purple and green photosynthetic bacteria, it was supposed that such organisms lacked the oxygen-forming system and, instead, ‘OH’ was disposed of by reduction with an inorganic H(e) donor (other than water) according to the general equation:
$$2 'OH' + H_2 A \to 2 H_2 O + A ,$$
where H2A is H2 or an inorganic sulfur compound.

Critical tests of van Niel's hypothesis could not be devised, and his proposal was abandoned soon after the discovery of in vitro photophosphorylation by green plant chloroplasts and membranes of purple bacteria in 1954. Photophosphorylation was then viewed as one key common denominator of oxygenic and anoxygenic photosyntheses. From later research it became clear that light-dependent phosphorylation of adenosine diphosphate was a consequence of photochemical charge separation and electron flow in reaction centers embedded in membranes of all photosynthetic organisms. The similarities, as well as the differences, in fine structure and function of reaction centers in anoxygenic and oxygenic organisms are now believed to reflect the course of evolution of oxygenic organisms from anoxygenic photosynthetic precursors. Thus, with the acquisition of new knowledge, concepts of the comparative biochemistry of photosynthetic processes have been radically altered during the past several decades. This paper describes highpoints of the history of these changes.

Key words

comparative biochemistry alternative modes of photosynthesis 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arnon DI (1991) Photosynthetic electron transport: Emergence of a concept, 1949–59. Photosynth Res 29: 117–131Google Scholar
  2. Arnon DI, Allen MB, and Whatley FR (1954) Photosynthesis by isolated chloroplasts. Nature (London) 174: 394–396Google Scholar
  3. Aronoff S and Calvin M (1948) Phosphorus turnover and photosynthesis. Plant Physiol 23: 351–358Google Scholar
  4. Baas-Becking LGM and Parks GS (1927) Energy relations in the metabolism of autotrophic bacteria. Physiol Rev 7: 85–106Google Scholar
  5. Beer-Romero P and Gest H (1987)Heliobacillus mobilis, a peritrichously flagellated anoxyphototroph containing bacteriochlorophyllg. FEMS Microbiol Lett 41: 109–114Google Scholar
  6. Beer-Romero P, Favinger JL and Gest H (1988) Distinctive properties of bacilliform photosynthetic heliobacteria. FEMS Microbiol Lett 49: 451–454Google Scholar
  7. Blankenship RE (1992) Origin and early evolution of photosynthesis. Photosynth Res 33: 91–111PubMedGoogle Scholar
  8. Blum HF (1937) On the evolution of photosynthesis. Amer Naturalist 71: 350–362Google Scholar
  9. Bose SK and Gest H (1963) Relationships between energygeneration and net electron transfer in bacterial photosynthesis. In: Chance B (ed) Energy-linked Functions of Mitochondria, pp 207–218. Academic Press, New YorkGoogle Scholar
  10. Cohen SS (1963) On biochemical variability and innovation. Science 139: 1017–1026PubMedGoogle Scholar
  11. Cohen-Bazire G, Sistrom WR and Stanier RY (1957) Kinetic studies of pigment synthesis by non-sulfur purple bacteria. J Cell Comp Physiol 49: 25–68Google Scholar
  12. Duysens LNM (1989) The discovery of the two photosynthetic systems: A personal account. Photosynth Res 21: 61–79Google Scholar
  13. Foster JW (1940) The role of organic substrates in photosynthesis of purple bacteria. J Gen Physiol 24: 123–134Google Scholar
  14. Frenkel AW (1954) Light-induced phosphorylation by cell-free preparations of photosynthetic bacteria. J Am Chem Soc 76: 5568–5569Google Scholar
  15. Fuller RC, Sprague SG, Gest H, and Blankenship RE (1985) A unique photosynthetic reaction center fromHeliobacterium chlorum. FEBS Lett 182: 345–349Google Scholar
  16. Gest H (1951) Metabolic patterns in photosynthetic bacteria. Bacteriol Revs 15: 183–210Google Scholar
  17. Gest H (1966) Comparative biochemistry of photosynthetic processes. Nature (London) 209: 879–882Google Scholar
  18. Gest H (1982) The comparative biochemistry of photosynthesis: Milestones in a conceptual zigzag. In: Kaplan NO and Robinson A (eds) Cyclotrons to Cytochromes, Essays in Molecular Biology and Chemistry, pp 305–321. Academic Press, New YorkGoogle Scholar
  19. Gest H (1988) Sun-beams, cucumbers, and purple bacteria. Photosynth Res 19: 287–308Google Scholar
  20. Gest H (1991) The legacy of Hans Molisch (1856–1937), photosynthesis savant. Photosynth Res 30: 49–59Google Scholar
  21. Gest H and Favinger JL (1983)Heliobacterium chlorum, an anoxygenic brownish-green photosynthetic bacterium containing a ‘new’ form of bacteriochlorophyll. Arch Microbiol 136: 11–16Google Scholar
  22. Gest H and Kamen MD (1948) Studies on the phosphorus metabolism of green algae and purple bacteria in relation to photosynthesis. J Biol Chem 176: 299–318Google Scholar
  23. Harold FM (1986) The Vital Force: A Study of Bioenergetics. WH Freeman, New YorkGoogle Scholar
  24. Hill R (1937) Oxygen evolved by isolated chloroplasts. Nature (London) 139: 881–882Google Scholar
  25. Hill R (1939) Oxygen produced by isolated chloroplasts. Proc Roy Soc B 127: 192–210Google Scholar
  26. Ingen-Housz J (1779) Experiments upon Vegetables, Discovering Their great Power of purifying the Common Air in the Sun-shine and of Injuring it in the Shade and at Night, to which is joined a new Method of examining the accurate Degree of Salubrity of the Atmosphere. Printed for P. Elmsly in the Strand and H. Payne in Pall Mall, LondonGoogle Scholar
  27. Kluyver AJ and Donker HJL (1926) Die Einheit in der Biochimie. Chem Zelle Gewebe 13: 134–190Google Scholar
  28. Levitt LS (1953) Photosynthesis as a photoelectric phenomenon. Science 118: 696–697PubMedGoogle Scholar
  29. Levitt LS (1954) The role of magnesium in photosynthesis. Science 120: 33–35PubMedGoogle Scholar
  30. Madigan MT (1992) The family Heliobacteriaceae. In: Balows A, Trüper HG, Dworkin M, Harder W and Schleifer K-H (eds) The Prokaryotes, 2nd Ed, Vol II, pp 1981–1992. Springer Verlag, New York, BerlinGoogle Scholar
  31. McKie D (1952) Antoine Lavoisier: Scientist, Economist, Social Reformer. Da Capo Press, New YorkGoogle Scholar
  32. Mechalas BJ and Rittenberg SC (1960) Energy coupling inDesulfovibrio desulfuricans. J Bacteriol 80: 501–507PubMedGoogle Scholar
  33. Molisch H (1907) Die Purpurbakterien nach neuen Untersuchungen. Gustav Fischer, JenaGoogle Scholar
  34. Myers J (1974) Conceptual developments in photosynthesis, 1924–1974. Plant Physiol 54: 420–426Google Scholar
  35. Nitschke W and Rutherford AW (1991) Photosynthetic reaction centres: Variations on a common structural theme? Trends Biochem Sci 16: 241–245PubMedGoogle Scholar
  36. Ormerod JG and Gest H (1962) Hydrogen photosynthesis and alternative metabolic pathways in photosynthetic bacteria. Bacteriol Revs 26: 51–66Google Scholar
  37. Poincaré H (1905/1952) Science and Hypothesis, p 147. Dover Publications, Inc., New York. Republication of the first English translation published in 1905 by the Walter Scott Publishing Co, LtdGoogle Scholar
  38. Prince RC, Gest H and Blankenship RE (1985) Thermodynamic properties of the photochemical reaction center ofHeliobacterium chlorum. Biochim Biophys Acta 810: 377–384Google Scholar
  39. Ruben S (1943) Photosynthesis and phosphorylation. J Am Chem Soc 65: 279–282Google Scholar
  40. Trost JT, Brune DC and Blankenship RE (1992) Protein sequences and redox titrations indicate that the electron acceptors in reaction centers from heliobacteria are similar to Photosystem I. Photosynth Res 32: 11–22PubMedGoogle Scholar
  41. van deMeent EJ, Kobayashi M, Erkelens C, vanVeelen PA, Amesz J and Watanabe T (1991) Identification of 81-hydroxy chlorophylla as a functional reaction center pigment in heliobacteria. Biochim Biophys Acta 1058: 356–362Google Scholar
  42. vanNiel CB (1930) Photosynthesis of bacteria. In: Contributions to Marine Biology, pp 161–169. Stanford Univ Press, StanfordGoogle Scholar
  43. vanNiel CB (1932) On the morphology and physiology of the purple and green sulphur bacteria. Arch Mikrobiol 3: 1–112Google Scholar
  44. vanNiel CB (1935) Photosynthesis of bacteria. Cold Spring Harbor Symp. Quant Biol 3: 138–150Google Scholar
  45. vanNiel CB (1941) The bacterial photosyntheses and their importance for the general problem of photosynthesis. Advan Enzymol 1: 263–328Google Scholar
  46. vanNiel CB (1944) The culture, general physiology, morphology and classification of the non-sulfur purple and brown bacteria. Bacteriol Revs 8: 1–118Google Scholar
  47. vanNiel CB (1949) The comparative biochemistry of photosynthesis. In: Franck J and Loomis WE (eds) Photosynthesis in Plants, pp 437–495. Iowa State College Press, AmesGoogle Scholar
  48. vanNiel CB (1956) Phototrophic bacteria; key to the understanding of green-plant photosynthesis. In: AJKluyver and CBvanNiel, The Microbe's Contribution to Biology, Harvard University Press, Cambridge, MassachusettsGoogle Scholar
  49. vanNiel CB (1967) The education of a microbiologist; some reflections. Ann Rev Microbiol 21: 1–30Google Scholar
  50. Wellington CL, Bauer CE, and Beatty JT (1992) Photosynthesis gene superoperons in purple non-sulfur bacteria: The tip of the iceberg? Can J Microbiol 38: 20–27Google Scholar
  51. Wurmser R (1930) Oxydations et Réductions. Les Presses Universitaires de France, Paris.Google Scholar
  52. Wurmser R (1987) Letter to the editor. Photosynth Res 13: 91–9Google Scholar

Copyright information

© Kluwer Academic Publishers 1993

Authors and Affiliations

  • Howard Gest
    • 1
    • 2
  1. 1.Photosynthetic Bacteria Group, Biology DepartmentIndiana UniversityBloomingtonUSA
  2. 2.Department of History and Philosophy of ScienceIndiana UniversityBloomingtonUSA

Personalised recommendations