Evolution of Photosynthesis

John F Allen, University of London, London, UK
Wim FJ Vermaas, Arizona State University, Tempe, Arizona, USA

Published online: October 2010

DOI: 10.1002/9780470015902.a0002034.pub2

Photosynthesis is the conversion of radiant energy, as light, into stored chemical energy. The central process is a light-driven separation of electrical charge across a biological membrane. Photochemical reaction centres carry out this process, and their three-dimensional protein structures now indicate that all modern reaction centres are homologous. Reaction centres with light-harvesting complexes comprise photosynthetic units, two of which are required for the oxygenic photosynthesis that now dominates biological energy flow in the biosphere. The evolutionary origin of oxygenic photosynthesis in cyanobacteria had a profound effect on the chemistry of the Earth's atmosphere, on geology and on biology, paving the way for the evolution of complex, multicellular life. Eukaryotic plants and algae maintain the descendents of cyanobacteria as specialised, subcellular, cytoplasmic organelles called chloroplasts. The genes that remain in chloroplasts may be retained to be subject to regulatory control by the photosynthetic electron transport chain.

Key Concepts:

  • Photochemical reaction centres trap absorbed light energy as transmembrane charge separation.
  • This vectorial electron transfer forms part of an electron transport chain, and drives vectorial proton translocation, establishing a proton motive force.
  • The proton motive may also be produced by nonphotosynthetic electron transfer and perhaps, originally, by geothermal convection in the first living cells. Photosynthesis may have originated as a light-driven supplement to vectorial metabolism.
  • Photochemical reaction centres today come in two broad types, I and II. These differ in their mode of electron transport, but the three-dimensional structure of their proteins indicates a common origin.
  • Type I and type II reaction centres originated by gene duplication and subsequently diverged to give the reaction centres found today in different lineages of anoxygenic, photosynthetic bacteria, each with a single type of reaction centre.
  • Type I and type II reaction centres came together again, in the first cyanobacterium, as photosystem I and photosystem II, two mutually interdependent photosynthetic units connected in series.
  • Photosystem I and photosystem II together generate a sufficiently large electrical potential difference to permit photo-oxidation of water and photo-reduction of NADP+, with a consequent liberation of molecular oxygen.
  • Oxygenic photosynthesis was acquired by eukaryotic cells through endosymbiosis with cyanobacteria.
  • The overwhelming majority of cyanobacterial genes were either lost or relocated to the plant cell nucleus.
  • Control of gene expression by photosynthetic electron transport may be an absolute and continuing requirement that justifies the maintenance of the small, quasi-autonomous, chloroplast genetic system.

Keywords: photosynthetic reaction centres; light-harvesting antenna complexes; chlorophyll-binding proteins; electron transport; chloroplast; photosynthetic bacteria; cyanobacteria; photosystem I; photosystem II; oxygen evolution

Figure 1. Generic model of a photosynthetic reaction centre in a membrane. The reaction centre consists of a homodimer or heterodimer of polypeptides (indicated by rectangles) that bind cofactors involved in electron transfer. A central component in the photosynthetic reaction centre is the primary donor, indicated by (Chl)2, which is a dimer of chlorophyll a or one of its derivatives (such as a bacteriochlorophyll). Upon excitation by light energy, the primary donor transfers an electron through a chlorophyll (or derivative), ChlA, to another pigment, indicated by ChlB, which may be a (bacterio)pheophytin or a (bacterio)chlorophyll. This electron transfer takes place within 3–30 ps. Depending on the type of reaction centre, electron transfer can involve one or both of the pathways present in the dimeric reaction centre. In photosystem I-type reaction centres, electrons may flow along both branches (arrows with solid or dotted lines) through the chlorophylls to quinones (QA or QB) and then to an iron–sulfur centre (FeS) and subsequent acceptors (A) on the cytoplasmic/stromal side of the membrane, without necessarily involving the other quinone in electron transfer. In photosystem II-type reaction centres, however, only one of the branches is used (solid lines), and the two Chls at the right are not involved in electron transfer; they are said to be on the inactive branch of the electron transport chain. The electron in photosystem II-type reaction centres is transferred from QA to QB through a nonhaem iron (Fe) and then to an acceptor (A) (such as another quinone) in the membrane. In both types of reaction centres, the oxidised primary donor is rereduced by a donor D, which may be either in the membrane or on the lumenal/periplasmic side of the membrane.
Figure 2. Electron transfer scheme for photosystem II-type (left) and photosystem I-type (right) reaction centres. Vertically, the electron transport components have been arranged according to their redox midpoint potential. A more negative midpoint potential means that components are stronger electron donors (reductants), and a more positive potential is indicative of a stronger oxidant. The two examples of photosystem II-type reaction centres indicated in this scheme are those from Rhodobacter sphaeroides, a purple nonsulfur bacterium (left), and photosystem II (middle left). The two examples of photosystem I-type reaction centres shown here are photosystem I (middle right) and the reaction centre from Chlorobium tepidum, a green sulfur bacterium (right). Abbreviations: A1, quinone-type electron acceptor (vitamin K1 in photosystem I and in C. tepidum); BChl, bacteriochlorophyll; BPheo, bacteriopheophytin; Chl, chlorophyll; cyt, cytochrome; FA, FB and FX, Fe4S4 centres; Fd, ferredoxin; hv, light; P870, P680, P700 and P840, the primary donors (Bchl a, Chl a, Chl a/a¢ and BChl a, respectively) in the reaction centres of R. sphaeroides, photosystem II, photosystem I and C. tepidum, respectively; PC, plastocyanin; Pheo, pheophytin (chlorophyll without a central magnesium ions) and QA and QB, the primary and secondary quinone-type electron acceptors (these quinones are ubiquinones in Rhodobacter, and plastoquinone in photosystem II).
Figure 3. Possible structural homology between type II reaction centres and cytochrome b, as proposed by Xiong et al. (2000). Haem groups (red) of cytochrome b become substituted by chlorin rings (green) of (bacterio)chlorophyll and (bacterio)phaeophytin in the transition from cytochrome to reaction centre and occupy positions spanning the membrane by means of ligation to conserved histidine side chains (blue).
Figure 4. A possible evolutionary relationship between reaction centres and light-harvesting complexes. Initially, two small pigment-binding membrane proteins, each with a single membrane-spanning helix, may have given rise to a simple reaction centre by gene duplication, divergence and possibly fusion. Other but perhaps similar pigment-binding membrane proteins may have undergone duplication, divergence and fusion events, leading to multihelix core antenna proteins. Fusion of a core antenna and a reaction centre protein is expected to have led to homodimeric photosystem I-type reaction centres such as those of heliobacteria. The homodimeric reaction centres may have evolved to heterodimeric ones by another round of gene duplication and divergence. Core antenna proteins and five-helix reaction centre proteins may have duplicated to form heterodimeric photosystem II-type reaction centre complexes. Reaction centres from purple bacteria may have formed by combination of a heterodimeric photosystem II-type reaction centre with single-helix antenna proteins, possibly similar to one of the ancestral one-helix pigment-binding proteins.
Figure 5. Relationship between type I and type II reaction centres based on numbers and origin of their component transmembrane helices. A type II reaction centre has its origin in cytochrome b (as in Figure 3), and the core of the reaction centre consists of five membrane-spanning helices A to E. Gene fusion leads to addition of six additional helices (a to f) from a light-harvesting antenna protein to form the larger reaction centre core of type I reaction centres, including photosystem I.
Figure 6. Retention of type I and type II centres, selected by a redox switch. Adapted from Allen (2005). Type I (RC I) and type II (RC II) reaction centres separate, allowing specialisation and eventual loss of the redundant reaction centre in photoautochemotrophic (type I-containing) lineages (e.g. Chlorobium and Heliobacillus spp.) and in photoheteroorganotrophic (type II-containing) lineages (e.g. Rhodobacter, Rhodospirillum spp.). However, a versatile, facultatively chemoautotrophic photosynthetic bacterium retains genes for both type I and type II reaction centres. In this hypothetical ancestor of cyanobacteria and chloroplasts, expression of type I centre genes in the presence of hydrogen sulfide is accompanied by silent type II genes. Type II genes are themselves induced under nonreducing conditions, when type I genes become repressed. Eventually, loss of regulatory control allows coexistence of type I and type II reaction centres, with complementary functions. In place of hydrogen sulfide, the type II centre, as photosystem II (PS II), oxidises water, liberating oxygen, and donating electrons to the type I centre, as photosystem I (PS I).
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    book Morton O (2007) Eating the Sun: How Plants Power the Planet. London: Fourth Estate.
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Related Sub-Topics:

Evolution of Novelty | Molecular Evolution | Protein Evolution | Evolution of Coding and Functional Modules | Plant Evolution | Photosynthesis
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Article Title: Evolution of Photosynthesis
 
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Allen, John F, and Vermaas, Wim FJ(Oct 2010) Evolution of Photosynthesis. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0002034.pub2]