PP62CH21-Blankenship ARI 15 April 2011 10:14 Evolution of Photosynthesis Martin F. Hohmann-Marriott1 and Robert E. Blankenship2 1Department of Biochemistry, University of Otago, Dunedin 9016, New Zealand 2Departments of Biology and Chemistry, Washington University in St. Louis, St. Louis, Missouri 63130; email: [email protected] Annu. Rev. Plant Biol. 2011. 62:515–48 Keywords First published online as a Review in Advance on oxygen, reaction center, chlorophyll, chemiosmosis, electron March 23, 2011 transport, endosymbiosis The Annual Review of Plant Biology is online at plant.annualreviews.org Abstract This article’s doi: Energy conversion of sunlight by photosynthetic organisms has changed 10.1146/annurev-arplant-042110-103811 Earth and life on it. Photosynthesis arose early in Earth’s history, and Copyright c 2011 by Annual Reviews. the earliest forms of photosynthetic life were almost certainly anoxy- by Universidad Veracruzana on 01/08/14. For personal use only. All rights reserved genic (non-oxygen evolving). The invention of oxygenic photosynthesis 1543-5008/11/0602-0515$20.00 and the subsequent rise of atmospheric oxygen approximately 2.4 bil- Annu. Rev. Plant Biol. 2011.62:515-548. Downloaded from www.annualreviews.org lion years ago revolutionized the energetic and enzymatic fundamen- tals of life. The repercussions of this revolution are manifested in novel biosynthetic pathways of photosynthetic cofactors and the modifica- tion of electron carriers, pigments, and existing and alternative modes of photosynthetic carbon fixation. The evolutionary history of pho- tosynthetic organisms is further complicated by lateral gene transfer that involved photosynthetic components as well as by endosymbiotic events. An expanding wealth of genetic information, together with bio- chemical, biophysical, and physiological data, reveals a mosaic of pho- tosynthetic features. In combination, these data provide an increasingly robust framework to formulate and evaluate hypotheses concerning the origin and evolution of photosynthesis. 515 PP62CH21-Blankenship ARI 15 April 2011 10:14 pigments engaged in harvesting sunlight. An at- Contents mosphere in which large amounts of complex organic molecules and high concentrations of INTRODUCTION.................. 516 oxygen coexist (106) is another sign that the TheEnergeticsofPresentLife..... 516 entire planet is bustling with life. Over billions Energetics of the Early Period in of years, photosynthetic organisms have trans- LifeHistory.................... 517 formed our planet and the life on it (30). The The Quest for Carbon . 517 interdependence of photosynthesis and the de- Proton and Electron Transport . 517 velopment of our planet and the life it harbors Distribution of Photosystems make the study of the evolutionary develop- and Rhodopsins. 518 ment of photosynthesis an exciting endeavor This Review . 518 that connects experimental data and theoreti- GEOLOGICAL EVIDENCE FOR cal concepts across scientific disciplines. PHOTOSYNTHESIS............. 518 CarboninAncientRocks........... 519 Oxygen............................ 519 The Energetics of Present Life Fossil Record . 520 Life requires a constant flux of energy to persist Chemical Indicators. 520 and proliferate. The energy gradient that main- GeneticEvidence.................. 520 tains our biosphere is provided by photosyn- MECHANISMS OF EVOLUTION . 521 thesis. Photosynthetic organisms stabilize the Molecular Evolution . 521 fleeting energy contained in a photon by break- Establishing Metabolic Networks . 521 ing and creating chemical bonds against the EVOLUTION OF COFACTORS . 521 chemical equilibrium. Our present atmosphere IronSulfurCluster................. 521 composition, with more than 20% O2, provides Hemes............................ 522 the basis of the energy gradient that sustains life Quinones.......................... 522 close to the Earth’s surface (147). The domi- Chlorophylls...................... 524 nant group of photosynthetic organisms gen- EVOLUTION OF PROTEIN erates O2 through the decomposition of water. COMPLEXES.................... 527 The electrons liberated in this process can be Rhodopsins . 527 used to reduce inorganic carbon to form organic Reaction Centers . 527 molecules to build cellular components. This ATPSynthases.................... 532 stored redox energy can be released by oxidizing Light-Harvesting Complexes . 534 the generated molecules, thereby recombining by Universidad Veracruzana on 01/08/14. For personal use only. Quinol-Acceptor Oxidoreductase . 535 electrons with O2 and protons to generate wa- EVOLUTION OF ORGANISM ter. This process is the basis of energy gener- GROUPS......................... 536 Annu. Rev. Plant Biol. 2011.62:515-548. Downloaded from www.annualreviews.org ation by oxygen-dependent respiration. Pho- Evolution of Photosynthetic tosynthesis and oxygen-dependent respiration Bacteria........................ 536 complete a water-oxygen cycle (46). Before wa- Evolution of Photosynthetic ter was adopted as the main electron source, Eukaryotes..................... 536 photosynthetic organisms may have utilized hy- PERSPECTIVE...................... 540 drogen, ferrous iron, and hydrogen sulfide in place of oxygen as an electron source for redox cycling (Table 1), and even today many types of anoxygenic (non-oxygen-evolving) photosyn- INTRODUCTION thetic organisms utilize these electron donors Our planet is alive and photosynthesis pow- instead of water. The continued utilization ers it. This is evident by the spectral signa- of oxygen, sulfur, and iron, in combination ture of our planet (96), which is colored by the with the incorporation of inorganic carbon, left 516 Hohmann-Marriott · Blankenship PP62CH21-Blankenship ARI 15 April 2011 10:14 signatures for tracing the early evolution of life Table 1 Redox midpoint potentials of electron donor and electron and metabolic processes such as photosynthesis carrier redox couples through geological times (74). Redox midpoint Reductant Redox couple potential at pH 7 [V] a + − Energetics of the Early Period Hydrogen H2/2H 0.420 a 0 − in Life History Sulfide H2S/S 0.240 b,c 2+ Ferrous iron Fe /Fe(OH)3 0.150 Virtually all oxygen in our atmosphere has a Hydrogen peroxide H2O2/O2 0.270 been produced by oxygenic photosynthetic a Water H2O/1/2 O2 0.815 organisms. However, for long periods in the Ferredoxin (red)a Fd (red)/Fd (ox) −0.430 history of our planet and life, oxygen may not NADPHa NADPH/NADP −0.320 have been present in the atmosphere to an ap- Menaquinold MQ (red)/MQ (ox) −0.070 preciable extent (80). The ancient atmosphere Ubiquinold UQ (red)/UQ (ox) 0.100 was composed of methane, carbon dioxide, and Plastoquinold PQ (red)/PQ (ox) 0.100 nitrogen. The organisms that lived then did Rieske FeS clusterc RFeS (red)/RFeS (ox) 0.100–0.270 not rely on the oxygen–water cycle but were linked to other molecules in a strictly anaerobic aSee Reference 121. biochemistry. When O2 appeared in the atmo- bSee Reference 118. sphere approximately 2.4 Gya, it fundamentally cAt 10 μML−1. altered the redox balance on Earth, and or- dSee Reference 160. ganisms were either forced to adapt to oxygen, retreat to anaerobic ecological niches, or be- (RCs) provide electrons for photoautotrophic come extinct. Evolving ways to tolerate O2 and eventually to utilize the tremendous amount of organisms, including green sulfur bacteria, most purple bacteria, cyanobacteria, and energy available when O2 is used as a terminal oxidant, organisms greatly expanded their photosynthetic eukaryotes. In contrast, photo- repertoire of metabolic processes (29, 152). heterotrophic organisms, including some types of purple bacteria, acidobacteria, heliobacteria, and some photosynthetic Archaea, utilize light The Quest for Carbon energy to generate a protonmotive force and The ability to create organic molecules by phosphoanhydride bonds but require organic incorporating inorganic carbon is critical molecules as a carbon source. A schematic to carbon-based life forms. Creatures that of different modes of light-driven energy by Universidad Veracruzana on 01/08/14. For personal use only. can do it without using organic molecules conversion is given in Figure 1. produced by others are endowed with the Gya: giga (1 × 109) Annu. Rev. Plant Biol. 2011.62:515-548. Downloaded from www.annualreviews.org title “autotroph.” Different pathways for the incorporation of carbon exist (171) (Table 1). Proton and Electron Transport years ago Some organisms grow autotrophically on The flow of electrons—from electron donor Autotroph: an methane that is oxidized to generate energy as to electron acceptor—is channeled by protein organism that can produce all carbon- well as to provide the carbon for incorporation complexes that always contain metallo-organic containing molecules into cellular metabolism (173) by aerobic and cofactors. Although dissipating this energy gra- from small, inorganic oxygen-independent respiration (145). In con- dient can store energy by generating or break- molecules utilizing chemical energy trast to CH4 incorporation, where getting rid ing chemical bonds, another mechanism for of electrons is the tricky part, the incorporation capturing energy is ubiquitous throughout the gradients (chemoautotroph) or of CO2 requires electrons. Electron donors in tree of life. Membrane-bound complexes cou- light energy the environment are the staple electron source ple the transfer of electrons across the mem- (photoautotroph) for chemoautotrophic organisms, and elec- brane to the generation