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

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.