Evolution of Photosynthesis

Abstract

Photosynthesis originated once during the early Archaean due to the emergence of photochemical reaction centres, the biological nanomachines that convert the energy of light into chemical energy. The evolution of the photosynthetic machinery is consistent with a single origin of photosynthesis followed by an early diversification event that resulted in the rapid evolution of distinct reaction centre types and pigment forms. One of these reaction centres specialised in highly oxidising photochemistry, which facilitated the oxidation of Mn and the evolution of the water‐oxidising cluster of Photosystem II. In addition, the last common ancestor of all photosynthetic organisms can be traced back to a period of time near the root or at the root of the tree of life of bacteria, with the current distribution of photosynthesis being the result of widespread loss of photosynthetic capacity and horizontal gene transfer.

Key Concepts

  • Photosynthesis originated at least 3.5 billion years ago, but it could be much older.
  • Photosynthesis evolved only once in ancestral forms of bacteria.
  • Type I and Type II reaction centres originated from an ancestral gene duplication event.
  • The last common ancestor of photosynthetic bacteria had type I and type II reaction centres.
  • Photosystem II originated from the close interaction of a Type I and Type II reaction centre.
  • The ancestral homodimeric Photosystem II was able to catalyse the oxidation of water.
  • The last common ancestor of photosynthetic bacteria had protochlorophyllide and chlorophyllide reductase and could make pigments similar to chlorophyll a and bacteriochlorophyll g.
  • Nitrogenase and the chlorophyll synthesis enzymes originated from an ancient gene duplication event predating the diversification of bacteria.
  • The current distribution of photosynthesis in bacteria is explained by widespread loss of photosynthesis and horizontal gene transfer.

Keywords: photochemical reaction centre; photosystem; water oxidation; water‐oxidising complex; chlorophyll; photochemistry; Archaean; Great Oxidation Event; cyanobacteria

Figure 1. The Mn4CaO5 cluster of Photosystem II. (a, b) Ligands surrounding the cluster; those provided by the D1 reaction centre protein are coloured grey and those provided by the CP43 subunit are shown in orange. The magenta spheres represent Mn; green, Ca and red, O. (c) Location of the ligands to the cluster in relation to the protein scaffold; the CP43 subunit is shown in orange, while the D1 subunit is shown in grey.
Figure 2. Comparison of reaction centre subunits and their cofactors. (a–c) The core of the anoxygenic Type II reaction centre from the proteobacterium Thermochromatium tepidum, PDB: 3WMM. (d–f) The core of Photosystem II from the cyanobacterium Thermosynechococcus vulcanus, PDB: 3WU2. (g–i) The core domain of Photosystem I from Thermosynechococcus elongatus, PDB: 1JB0. Panels (a, d, g) show the protein scaffold highlighting the five transmembrane helices of the reaction centre core. Panels (b, e, h) show the cofactors involved in photochemistry; QB and FX mark the position of the terminal electron acceptor. Panels (c, f, i) show the cofactors embedded within the protein scaffold.
Figure 3. Structural similarities between Photosystem I (a, b) and Photosystem II (c, d). The core antenna is highlighted in light blue and the reaction centre core in transparent grey and orange. In Photosystem I and the other Type I reaction centres, the antenna and reaction centre core are a single protein, while in Photosystem II these are individual proteins. Therefore, the core of Photosystem I is made of two subunits, each one with an antenna and a reaction centre domain (PsaA and PsaB). On the other hand, the core of Photosystem II is made of four subunits, two containing the antenna domain (CP43 and CP47) and two containing the reaction centre domain (D1 and D2). The CP43 and CP47 subunits originated from a Type I reaction centre protein. In panels (a) and (c), the two peripheral chlorophylls that connect the antenna with the reaction centre are highlighted as spheres. They occupy strictly homologous positions and are coordinated by conserved histidine residues located in the reaction centre domain. This indicates that they were present in the primordial reaction centre before the divergence of Type I and Type II forms. It can be concluded that Photosystem II is a chimera of both reaction centre types. The fact that these peripheral chlorophylls are present in Photosystem II strongly suggests that they have been retained since the origin of both reaction centres and implies that the core subunits that gave rise to D1 and D2 have always been in close contact with a Type I reaction centre. Anoxygenic Type II reaction centres lack these peripheral chlorophylls as they have a different antenna system lacking homologues to CP43 and CP47. (b, d) Details of the interaction between the antenna and the reaction centre core; green lines display light harvesting chlorophylls.
Figure 4. Comparison of protochlorophyllide reductase and nitrogenase. (a) Protochlorophyllide reductase from Prochlorococcus marinus, PDB: 2YNM. (b) Nitrogenase from Azotobacter vinelandii, PDB: 1N2C. Notice the similarities between both enzymatic complexes. The outermost orange cofactors within the L and H subunits represent ADP (adenosine diphosphate). The innermost cofactor in (a) represents protochlorophyllide.
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Cardona, Tanai(Jan 2017) Evolution of Photosynthesis. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0002034.pub3]