1932

Abstract

Photosystem II is the water-oxidizing and O-evolving enzyme of photosynthesis. How and when this remarkable enzyme arose are fundamental questions in the history of life that have remained difficult to answer. Here, recent advances in our understanding of the origin and evolution of photosystem II are reviewed and discussed in detail. The evolution of photosystem II indicates that water oxidation originated early in the history of life, long before the diversification of cyanobacteria and other major groups of prokaryotes, challenging and transforming current paradigms on the evolution of photosynthesis. We show that photosystem II has remained virtually unchanged for billions of years, and yet the nonstop duplication process of the D1 subunit of photosystem II, which controls photochemistry and catalysis, has enabled the enzyme to become adaptable to variable environmental conditions and even to innovate enzymatic functions beyond water oxidation. We suggest that this evolvability can be harnessed to develop novel light-powered enzymes with the capacity to carry out complex multistep oxidative transformations for sustainable biocatalysis.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-070522-062509
2023-05-22
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/arplant/74/1/annurev-arplant-070522-062509.html?itemId=/content/journals/10.1146/annurev-arplant-070522-062509&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alcott LJ, Mills BJW, Poulton SW. 2019. Stepwise Earth oxygenation is an inherent property of global biogeochemical cycling. Science 366:1333–37
    [Google Scholar]
  2. 2.
    Allen JP, Williams JC. 2011. The evolutionary pathway from anoxygenic to oxygenic photosynthesis examined by comparison of the properties of photosystem II and bacterial reaction centers. Photosynth. Res. 107:59–69
    [Google Scholar]
  3. 3.
    Antonaru LA, Cardona T, Larkum AWD, Nurnberg DJ. 2020. Global distribution of a chlorophyll f cyanobacterial marker. ISME J. 14:2275–87
    [Google Scholar]
  4. 4.
    Armstrong FA. 2008. Why did nature choose manganese to make oxygen?. Philos. Trans. R. Soc. B 363:1263–70
    [Google Scholar]
  5. 5.
    Ayliffe MA, Scott NS, Timmis JN. 1998. Analysis of plastid DNA-like sequences within the nuclear genomes of higher plants. Mol. Biol. Evol. 15:738–45
    [Google Scholar]
  6. 6.
    Bao H, Burnap RL. 2016. Photoactivation: the light-driven assembly of the water oxidation complex of photosystem II. Front. Plant Sci. 7:578
    [Google Scholar]
  7. 7.
    Battistuzzi FU, Hedges SB. 2009. A major clade of prokaryotes with ancient adaptations to life on land. Mol. Biol. Evol. 26:335–43
    [Google Scholar]
  8. 8.
    Beanland TJ. 1990. Evolutionary relationships between “Q-type” photosynthetic reaction centers: hypothesis-testing using parsimony. J. Theor. Biol. 145:535–45
    [Google Scholar]
  9. 9.
    Betts HC, Puttick MN, Clark JW, Williams TA, Donoghue PCJ, Pisani D. 2018. Integrated genomic and fossil evidence illuminates life's early evolution and eukaryote origin. Nat. Ecol. Evol. 2:1556–62
    [Google Scholar]
  10. 10.
    Blank CE, Sánchez-Baracaldo P. 2010. Timing of morphological and ecological innovations in the cyanobacteria—a key to understanding the rise in atmospheric oxygen. Geobiology 8:1–23
    [Google Scholar]
  11. 11.
    Blankenship RE. 1992. Origin and early evolution of photosynthesis. Photosynth. Res. 33:91–111
    [Google Scholar]
  12. 12.
    Blankenship RE, Parson WW. 1978. The photochemical electron transfer reactions of photosynthetic bacteria and plants. Annu. Rev. Biochem. 47:635–53
    [Google Scholar]
  13. 13.
    Blankenship RE, Sadekar S, Raymond J 2007. The evolutionary transition from anoxygenic to oxygenic photosynthesis. Evolution of Primary Producers in the Sea PG Falkowski, AH Knoll 21–35. Burlington, MA: Academic
    [Google Scholar]
  14. 14.
    Blum HF. 1937. On the evolution of photosynthesis. Am. Nat. 71:350–62
    [Google Scholar]
  15. 15.
    Boden JS, Konhauser KO, Robbins LJ, Sanchez-Baracaldo P. 2021. Timing the evolution of antioxidant enzymes in cyanobacteria. Nat. Commun. 12:4742
    [Google Scholar]
  16. 16.
    Boerner RJ, Nguyen AP, Barry BA, Debus RJ. 1992. Evidence from directed mutagenesis that aspartate 170 of the D1 polypeptide influences the assembly and/or stability of the manganese cluster in the photosynthetic water-splitting complex. Biochemistry 31:6660–72
    [Google Scholar]
  17. 17.
    Brinkert K, De Causmaecker S, Krieger-Liszkay A, Fantuzzi A, Rutherford AW. 2016. Bicarbonate-induced redox tuning in Photosystem II for regulation and protection. PNAS 113:12144–49Discovery of the function of bicarbonate at the acceptor side of photosystem II.
    [Google Scholar]
  18. 18.
    Brochier-Armanet C, Talla E, Gribaldo S. 2009. The multiple evolutionary histories of dioxygen reductases: implications for the origin and evolution of aerobic respiration. Mol. Biol. Evol. 26:285–97
    [Google Scholar]
  19. 19.
    Bryant DA, Hunter CN, Warren MJ. 2020. Biosynthesis of the modified tetrapyrroles—the pigments of life. J. Biol. Chem. 295:6888–925
    [Google Scholar]
  20. 20.
    Bryant DA, Shen G, Turner GM, Soulier N, Laremore TN, Ho MY. 2020. Far-red light allophycocyanin subunits play a role in chlorophyll d accumulation in far-red light. Photosynth. Res. 143:81–95
    [Google Scholar]
  21. 21.
    Campbell KA, Force DA, Nixon PJ, Dole F, Diner BA, Britt RD. 2000. Dual-mode EPR detects the initial intermediate in photoassembly of the photosystem II Mn cluster: the influence of amino acid residue 170 of the D1 polypeptide on Mn coordination. J. Am. Chem. Soc. 122:3754–61
    [Google Scholar]
  22. 22.
    Cao P, Pan X, Su X, Liu Z, Li M. 2020. Assembly of eukaryotic photosystem II with diverse light-harvesting antennas. Curr. Opin. Struct. Biol. 63:49–57
    [Google Scholar]
  23. 23.
    Cardona T. 2015. A fresh look at the evolution and diversification of photochemical reaction centers. Photosynth. Res. 126:111–34
    [Google Scholar]
  24. 24.
    Cardona T. 2016. Reconstructing the origin of oxygenic photosynthesis: Do assembly and photoactivation recapitulate evolution?. Front. Plant Sci. 7:257
    [Google Scholar]
  25. 25.
    Cardona T. 2017. Photosystem II is a chimera of reaction centers. J. Mol. Evol. 84:149–51
    [Google Scholar]
  26. 26.
    Cardona T. 2018. Early Archean origin of heterodimeric photosystem I. Heliyon 4:e00548
    [Google Scholar]
  27. 27.
    Cardona T. 2019. Thinking twice about the evolution of photosynthesis. Open Biol. 9:180246
    [Google Scholar]
  28. 28.
    Cardona T, Murray JW, Rutherford AW. 2015. Origin and evolution of water oxidation before the last common ancestor of the Cyanobacteria. Mol. Biol. Evol. 32:1310–28The first highly detailed evolutionary study of the D1 proteins of photosystem II.
    [Google Scholar]
  29. 29.
    Cardona T, Rutherford AW. 2019. Evolution of photochemical reaction centres: more twists?. Trends Plant Sci. 24:1008–21
    [Google Scholar]
  30. 30.
    Cardona T, Sánchez-Baracaldo P, Rutherford AW, Larkum AWD. 2019. Early Archean origin of photosystem II. Geobiology 17:127–50The first attempt at resolving the evolution of photosystem II and water oxidation as a function of time.
    [Google Scholar]
  31. 31.
    Cardona T, Sedoud A, Cox N, Rutherford AW. 2012. Charge separation in photosystem II: a comparative and evolutionary overview. Biochim. Biophys. Acta Bioenerg. 1817:26–43
    [Google Scholar]
  32. 32.
    Cardona T, Shao S, Nixon PJ. 2018. Enhancing photosynthesis in plants: the light reactions. Essays Biochem. 62:85–94
    [Google Scholar]
  33. 33.
    Castresana J, Saraste M. 1995. Evolution of energetic metabolism: the respiration-early hypothesis. Trends Biochem. Sci. 20:443–48
    [Google Scholar]
  34. 34.
    Catling DC, Zahnle KJ. 2020. The Archean atmosphere. Sci. Adv. 6:eaax1420
    [Google Scholar]
  35. 35.
    Chen C, Kazimir J, Cheniae GM. 1995. Calcium modulates the photoassembly of photosystem II (Mn)4-clusters by preventing ligation of nonfunctional high-valency states of manganese. Biochemistry 34:13511–26
    [Google Scholar]
  36. 36.
    Chen J-H, Wu H, Xu C, Liu X-C, Huang Z et al. 2020. Architecture of the photosynthetic complex from a green sulfur bacterium. Science 370:eabb6350
    [Google Scholar]
  37. 37.
    Chernev P, Fischer S, Hoffmann J, Oliver N, Assunção R et al. 2020. Light-driven formation of manganese oxide by today's photosystem II supports evolutionarily ancient manganese-oxidizing photosynthesis. Nat. Commun. 11:6110
    [Google Scholar]
  38. 38.
    Coleman GA, Davín AA, Mahendrarajah TA, Szánthó LL, Spang A et al. 2021. A rooted phylogeny resolves early bacterial evolution. Science 372:eabe0511
    [Google Scholar]
  39. 39.
    Crawford TS, Hanning KR, Chua JP, Eaton-Rye JJ, Summerfield TC. 2016. Comparison of D1′- and D1-containing PS II reaction centre complexes under different environmental conditions in Synechocystis sp. PCC 6803. Plant Cell Environ. 39:1715–26
    [Google Scholar]
  40. 40.
    Croce R, van Amerongen H. 2020. Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy. Science 369:eaay2058
    [Google Scholar]
  41. 41.
    Cser K, Vass I. 2007. Radiative and non-radiative charge recombination pathways in Photosystem II studied by thermoluminescence and chlorophyll fluorescence in the cyanobacterium Synechocystis 6803. Biochim. Biophys. Acta Bioenerg. 1767:233–43
    [Google Scholar]
  42. 42.
    David LA, Alm EJ. 2011. Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469:93–96
    [Google Scholar]
  43. 43.
    De Causmaecker S, Douglass JS, Fantuzzi A, Nitschke W, Rutherford AW. 2019. Energetics of the exchangeable quinone, QB, in Photosystem II. PNAS 116:19458–63
    [Google Scholar]
  44. 44.
    Demoulin CF, Lara YJ, Cornet L, Francois C, Baurain D et al. 2019. Cyanobacteria evolution: insight from the fossil record. Free Radic. Biol. Med. 140:206–23
    [Google Scholar]
  45. 45.
    Di Rienzi SC, Sharon I, Wrighton KC, Koren O, Hug LA et al. 2013. The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. eLife 2e01102Discovery of a nonphotosynthetic sister lineage of cyanobacteria.
  46. 46.
    Dong J, Fernandez-Fueyo E, Hollmann F, Paul CE, Pesic M et al. 2018. Biocatalytic oxidation reactions: a chemist's perspective. Angew. Chem. Int. Ed. Engl. 57:9238–61
    [Google Scholar]
  47. 47.
    Dong S, Huang G, Wang C, Wang J, Sui S-F, Qin X. 2022. Structure of the Acidobacteria homodimeric reaction center bound with cytochrome c. Nat. Commun. 13:7745
    [Google Scholar]
  48. 48.
    Ducluzeau AL, Schoepp-Cothenet B, van Lis R, Baymann F, Russell MJ, Nitschke W. 2014. The evolution of respiratory O2/NO reductases: an out-of-the-phylogenetic-box perspective. J. R. Soc. Interface 11:20140196
    [Google Scholar]
  49. 49.
    Fantuzzi A, Allgöwer F, Baker H, McGuire G, Teh WK et al. 2022. Bicarbonate-controlled reduction of oxygen by the QA semiquinone in Photosystem II in membranes. PNAS 119:e2116063119
    [Google Scholar]
  50. 50.
    Fournier GP, Moore KR, Rangel LT, Payette JG, Momper L, Bosak T. 2021. The Archean origin of oxygenic photosynthesis and extant cyanobacterial lineages. Proc. Biol. Sci. 288:20210675A state-of-the-art molecular clock analysis timing the evolution of cyanobacteria and using constraints from many horizontal gene transfer events.
    [Google Scholar]
  51. 51.
    Frei R, Crowe SA, Bau M, Polat A, Fowle DA, Døssing LN. 2016. Oxidative elemental cycling under the low O2 Eoarchean atmosphere. Sci. Rep. 6:21058
    [Google Scholar]
  52. 52.
    Gan F, Zhang S, Rockwell NC, Martin SS, Lagarias JC, Bryant DA. 2014. Extensive remodeling of a cyanobacterial photosynthetic apparatus in far-red light. Science 345:1312–17Discovery of the far-red light photoacclimation response involving extensive remodeling of the photosystems.
    [Google Scholar]
  53. 53.
    Garcia-Pichel F, Lombard J, Soule T, Dunaj S, Wu SH, Wojciechowski MF. 2019. Timing the evolutionary advent of cyanobacteria and the later Great Oxidation Event using gene phylogenies of a sunscreen. mBio 10:e00561-19
    [Google Scholar]
  54. 54.
    Garg H, Loughlin PC, Willows RD, Chen M. 2017. The C21-formyl group in chlorophyll f originates from molecular oxygen. J. Biol. Chem. 292:19279–89
    [Google Scholar]
  55. 55.
    Gisriel CJ, Azai C, Cardona T. 2021. Recent advances in the structural diversity of reaction centers. Photosynth. Res. 149:329–43
    [Google Scholar]
  56. 56.
    Gisriel CJ, Cardona T, Bryant DA, Brudvig GW. 2022. Molecular evolution of far-red light-acclimated photosystem II. Microorganisms 10:1270
    [Google Scholar]
  57. 57.
    Gisriel CJ, Sarrou I, Ferlez B, Golbeck JH, Redding KE, Fromme R. 2017. Structure of a symmetric photosynthetic reaction center–photosystem. Science 357:1021–25The first crystal structure of a homodimeric type I photosystem.
    [Google Scholar]
  58. 58.
    Gisriel CJ, Shen G, Ho MY, Kurashov V, Flesher DA et al. 2022. Structure of a monomeric photosystem II core complex from a cyanobacterium acclimated to far-red light reveals the functions of chlorophylls d and f. J. Biol. Chem. 298:101424
    [Google Scholar]
  59. 59.
    Gisriel CJ, Wang J, Liu J, Flesher DA, Reiss KM et al. 2022. High-resolution cryo-electron microscopy structure of photosystem II from the mesophilic cyanobacterium, Synechocystis sp. PCC 6803. PNAS 119:e2116765118
    [Google Scholar]
  60. 60.
    Granold M, Hajieva P, Tosa MI, Irimie FD, Moosmann B. 2018. Modern diversification of the amino acid repertoire driven by oxygen. PNAS 115:41–46
    [Google Scholar]
  61. 61.
    Grettenberger CL, Sumner DY, Wall K, Brown CT, Eisen JA et al. 2020. A phylogenetically novel cyanobacterium most closely related to Gloeobacter. ISME J. 14:2142–52
    [Google Scholar]
  62. 62.
    Gruber-Vodicka HR, Leisch N, Kleiner M, Hinzke T, Liebeke M et al. 2019. Two intracellular and cell type-specific bacterial symbionts in the placozoan Trichoplax H2. Nat. Microbiol. 4:1465–74
    [Google Scholar]
  63. 63.
    Hanson-Smith V, Kolaczkowski B, Thornton JW. 2010. Robustness of ancestral sequence reconstruction to phylogenetic uncertainty. Mol. Biol. Evol. 27:1988–99
    [Google Scholar]
  64. 64.
    Harada M, Akiyama A, Furukawa R, Yokobori SI, Tajika E, Yamagishi A. 2021. Evolution of superoxide dismutases and catalases in cyanobacteria: occurrence of the antioxidant enzyme genes before the rise of atmospheric oxygen. J. Mol. Evol. 89:527–43
    [Google Scholar]
  65. 65.
    Harel A, Karkar S, Cheng S, Falkowski PG, Bhattacharya D. 2015. Deciphering primordial cyanobacterial genome functions from protein network analysis. Curr. Biol. 25:628–34
    [Google Scholar]
  66. 66.
    Hays AM, Vassiliev IR, Golbeck JH, Debus RJ. 1998. Role of D1-His190 in proton-coupled electron transfer reactions in photosystem II: a chemical complementation study. Biochemistry 37:11352–65
    [Google Scholar]
  67. 67.
    Ho MY, Shen G, Canniffe DP, Zhao C, Bryant DA. 2016. Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science 353:aaf9178
    [Google Scholar]
  68. 68.
    Hohmann-Marriott MF, Blankenship RE 2011. Evolution of photosynthesis. Annu. Rev. Plant Biol. 62:515–48
    [Google Scholar]
  69. 69.
    Homann M, Heubeck C, Airo A, Tice MM. 2015. Morphological adaptations of 3.22 Ga-old tufted microbial mats to Archean coastal habitats (Moodies Group, Barberton Greenstone Belt, South Africa). Precambrian Res. 266:47–64
    [Google Scholar]
  70. 70.
    Hwang HJ, McLain A, Debus RJ, Bumap RL. 2007. Photoassembly of the manganese cluster in mutants perturbed in the high affinity Mn-binding site of the H2O-oxidation complex of photosystem II. Biochemistry 46:13648–57
    [Google Scholar]
  71. 71.
    Ishikita H, Saenger W, Biesiadka J, Loll B, Knapp EW. 2006. How photosynthetic reaction centers control oxidation power in chlorophyll pairs P680, P700, and P870. PNAS 103:9855–60
    [Google Scholar]
  72. 72.
    Jabłońska J, Tawfik DS. 2021. The evolution of oxygen-utilizing enzymes suggests early biosphere oxygenation. Nat. Ecol. Evol. 5:442–48A phylogenetic mapping of the origin of O2-using enzymes along the diversification of bacteria.
    [Google Scholar]
  73. 73.
    Johnson GN, Rutherford AW, Krieger A. 1995. A change in the midpoint potential of the quinone QA in Photosystem II associated with photoactivation of oxygen evolution. Biochim. Biophys. Acta Bioenerg. 1229:202–7
    [Google Scholar]
  74. 74.
    Johnson JE, Webb SM, Thomas K, Ono S, Kirschvink JL, Fischer WW. 2013. Manganese-oxidizing photosynthesis before the rise of cyanobacteria. PNAS 110:11238–43
    [Google Scholar]
  75. 75.
    Kanygin A, Milrad Y, Thummala C, Reifschneider K, Baker P et al. 2020. Rewiring photosynthesis: a photosystem I-hydrogenase chimera that makes H2in vivo. Energy Environ. Sci. 13:2903–14
    [Google Scholar]
  76. 76.
    Kasting JF, Walker JCG. 1981. Limits on oxygen concentration in the prebiological atmosphere and the rate of abiotic fixation of nitrogen. J. Geophys. Res. 86:1147–58
    [Google Scholar]
  77. 77.
    Kharecha P, Kasting J, Siefert J. 2005. A coupled atmosphere-ecosystem model of the early Archean Earth. Geobiology 3:53–76
    [Google Scholar]
  78. 78.
    Kimura M, Ota T. 1971. On the rate of molecular evolution. J. Mol. Evol. 1:1–17
    [Google Scholar]
  79. 79.
    Kiss E, Kós PB, Chen M, Vass I 2012. A unique regulation of the expression of the psbA, psbD, and psbE genes, encoding the D1, D2 and cytochrome b559 subunits of the Photosystem II complex in the chlorophyll d containing cyanobacterium Acaryochloris marina. Biochim. Biophys. Acta Bioenerg. 1817:1083–94
    [Google Scholar]
  80. 80.
    Knoops B, Loumaye E, Van Der Eecken V. 2007. Evolution of the peroxiredoxins. Subcell. Biochem. 44:27–40
    [Google Scholar]
  81. 81.
    Krieger A, Weis E, Demeter S 1993. Low-pH-induced Ca2+ ion release in the water-splitting system is accompanied by a shift in the midpoint redox potential of the primary quinone acceptor QA. Biochim. Biophys. Acta Bioenerg. 1144:411–18
    [Google Scholar]
  82. 82.
    Krynická V, Shao S, Nixon PJ, Komenda J. 2015. Accessibility controls selective degradation of photosystem II subunits by FtsH protease. Nat. Plants 1:15168
    [Google Scholar]
  83. 83.
    Kselíková V, Singh A, Bialevich V, Čížková M, Bišová K. 2022. Improving microalgae for biotechnology—from genetics to synthetic biology—moving forward but not there yet. Biotechnol. Adv. 58:107885
    [Google Scholar]
  84. 84.
    Magnabosco C, Moore KR, Wolfe JM, Fournier GP. 2018. Dating phototrophic microbial lineages with reticulate gene histories. Geobiology 16:179–89
    [Google Scholar]
  85. 85.
    Marchi S, Drabon N, Schulz T, Schaefer L, Nesvorny D et al. 2021. Delayed and variable late Archaean atmospheric oxidation due to high collision rates on Earth. Nat. Geosci. 14:827–31
    [Google Scholar]
  86. 86.
    Martin WF, Bryant DA, Beatty JT. 2018. A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiol. Rev. 42:205–31
    [Google Scholar]
  87. 87.
    Masuda T, Bernát G, Bečková M, Kotabová E, Lawrenz E et al. 2018. Diel regulation of photosynthetic activity in the oceanic unicellular diazotrophic cyanobacterium Crocosphaera watsonii WH8501. Environ. Microbiol. 20:546–60
    [Google Scholar]
  88. 88.
    Müh F, Glöckner C, Hellmich J, Zouni A. 2012. Light-induced quinone reduction in photosystem II. Biochim. Biophys. Acta Bioenerg. 1817:44–65
    [Google Scholar]
  89. 89.
    Mulo P, Sakurai I, Aro E-M. 2012. Strategies for psbA gene expression in cyanobacteria, green algae and higher plants: from transcription to PSII repair. Biochim. Biophys. Acta Bioenerg. 1817:247–57
    [Google Scholar]
  90. 90.
    Mulo P, Sicora C, Aro EM. 2009. Cyanobacterial psbA gene family: optimization of oxygenic photosynthesis. Cell. Mol. Life Sci. 66:3697–710
    [Google Scholar]
  91. 91.
    Murray JW. 2012. Sequence variation at the oxygen-evolving centre of Photosystem II: a new class of ‘rogue’ cyanobacterial D1 proteins. Photosynth. Res. 110:177–84
    [Google Scholar]
  92. 92.
    Nitschke W, Rutherford AW. 1991. Photosynthetic reaction centers: variations on a common structural theme?. Trends Biochem. Sci. 16:241–45
    [Google Scholar]
  93. 93.
    Nixon PJ, Diner BA. 1992. Aspartate 170 of the photosystem II reaction center polypeptide D1 is involved in the assembly of the oxygen-evolving manganese cluster. Biochemistry 31:942–48
    [Google Scholar]
  94. 94.
    Nurnberg DJ, Morton J, Santabarbara S, Telfer A, Joliot P et al. 2018. Photochemistry beyond the red limit in chlorophyll f-containing photosystems. Science 360:1210–13
    [Google Scholar]
  95. 95.
    Oliver N, Avramov AP, Nürnberg DJ, Dau H, Burnap RL. 2022. From manganese oxidation to water oxidation: assembly and evolution of the water-splitting complex in photosystem II. Photosynth. Res. 152:107–33
    [Google Scholar]
  96. 96.
    Oliver T, Sánchez-Baracaldo P, Larkum AW, Rutherford AW, Cardona T. 2021. Time-resolved comparative molecular evolution of oxygenic photosynthesis. Biochim. Biophys. Acta Bioenerg. 1862:148400
    [Google Scholar]
  97. 97.
    Olsen MT, Nowack S, Wood JM, Becraft ED, LaButti K et al. 2015. The molecular dimension of microbial species: 3. Comparative genomics of Synechococcus strains with different light responses and in situ diel transcription patterns of associated putative ecotypes in the Mushroom Spring microbial mat. Front. Microbiol. 6:604
    [Google Scholar]
  98. 98.
    Olson JM. 1970. The evolution of photosynthesis. Science 168438–46The first published scenario for the evolution of the photosystems.
  99. 99.
    Olson JM. 1981. Evolution of photosynthetic reaction centers. Biosystems 14:89–94
    [Google Scholar]
  100. 100.
    Olson JM, Blankenship RE. 2004. Thinking about the evolution of photosynthesis. Photosynth. Res. 80:373–86
    [Google Scholar]
  101. 101.
    Olson JM, Pierson BK. 1987. Evolution of reaction centers in photosynthetic prokaryotes. Int. Rev. Cytol. 108:209–48
    [Google Scholar]
  102. 102.
    Oparin AI, Braunshtein AE, Pasynski AG, Pavlovskaya TE. 1959. The Origin of Life on the Earth London: Pergamon
  103. 103.
    Ouzounis CA, Kunin V, Darzentas N, Goldovsky L. 2006. A minimal estimate for the gene content of the last universal common ancestor: exobiology from a terrestrial perspective. Res. Microbiol. 157:57–68
    [Google Scholar]
  104. 104.
    Park JJ, Lechno-Yossef S, Wolk CP, Vieille C 2013. Cell-specific gene expression in Anabaena variabilis grown phototrophically, mixotrophically, and heterotrophically. BMC Genom. 14:759
    [Google Scholar]
  105. 105.
    Parks DH, Chuvochina M, Rinke C, Mussig AJ, Chaumeil P-A, Hugenholtz P. 2022. GTDB: an ongoing census of bacterial and archaeal diversity through a phylogenetically consistent, rank normalized and complete genome-based taxonomy. Nucleic Acids Res. 50:D785–94
    [Google Scholar]
  106. 106.
    Pierson BK, Olson JM 1989. Evolution of photosynthesis in anoxygenic photosynthetic procaryotes. Microbial Mats: Physiological Ecology of Benthic Microbial Communities Y Cohen, E Rosenberg 402–27. Washington, DC: Am. Soc. Microbiol.
    [Google Scholar]
  107. 107.
    Planavsky NJ, Crowe SA, Fakhraee M, Beaty B, Reinhard CT et al. 2021. Evolution of the structure and impact of Earth's biosphere. Nat. Rev. Earth Environ. 2:123–39
    [Google Scholar]
  108. 108.
    Rahmatpour N, Hauser DA, Nelson JM, Chen PY, Villarreal A JC et al. 2021. A novel thylakoid-less isolate fills a billion-year gap in the evolution of Cyanobacteria. Curr. Biol. 31:2857–67.e4
    [Google Scholar]
  109. 109.
    Raven JA. 2009. Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquat. Microb. Ecol. 56:177–92
    [Google Scholar]
  110. 110.
    Reinhard CT, Planavsky NJ. 2022. The history of ocean oxygenation. Annu. Rev. Mar. Sci. 14:331–53
    [Google Scholar]
  111. 111.
    Rosing MT, Frei R. 2004. U-rich Archaean sea-floor sediments from Greenland–indications of >3700 Ma oxygenic photosynthesis. Earth Planet. Sci. Lett. 217:237–44
    [Google Scholar]
  112. 112.
    Rutherford AW. 1989. Photosystem II, the water-splitting enzyme. Trends Biochem. Sci. 14:227–32
    [Google Scholar]
  113. 113.
    Rutherford AW, Faller P. 2003. Photosystem II: evolutionary perspectives. Philos. Trans. R. Soc. B 358:245–53
    [Google Scholar]
  114. 114.
    Rutherford AW, Nitschke W. 1996. Photosystem 2 and the quinone–iron-containing reaction centers: comparisons and evolutionary perspectives. Origin and Evolution of Biological Energy Conversion H Baltscheffsky 143–75. New York: VCH
    [Google Scholar]
  115. 115.
    Rutherford AW, Osyczka A, Rappaport F. 2012. Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. FEBS Lett. 586:603–16
    [Google Scholar]
  116. 116.
    Satkoski AM, Beukes NJ, Li W, Beard BL, Johnson CM. 2015. A redox-stratified ocean 3.2 billion years ago. Earth Planet. Sci. Lett. 430:43–53
    [Google Scholar]
  117. 117.
    Sauer K. 1979. Photosynthesis—the light reactions. Annu. Rev. Phys. Chem. 30:155–78
    [Google Scholar]
  118. 118.
    Saw JH, Cardona T, Montejano G. 2021. Complete genome sequencing of a novel Gloeobacter species from a waterfall cave in Mexico. Genome Biol. Evol. 13:evab264
    [Google Scholar]
  119. 119.
    Schirrmeister BE, Sánchez-Baracaldo P, Wacey D. 2016. Cyanobacterial evolution during the Precambrian. Int. J. Astrobiol. 15:187–204
    [Google Scholar]
  120. 120.
    Schmidt-Rohr K. 2015. Why combustions are always exothermic, yielding about 418 kJ per mole of O2. J. Chem. Educ. 92:2094–99
    [Google Scholar]
  121. 121.
    Schmidt-Rohr K. 2021. O2 and other high-energy molecules in photosynthesis: why plants need two photosystems. Life 11:1191
    [Google Scholar]
  122. 122.
    Schubert WD, Klukas O, Saenger W, Witt HT, Fromme P, Krauss N. 1998. A common ancestor for oxygenic and anoxygenic photosynthetic systems: a comparison based on the structural model of photosystem I. J. Mol. Biol. 280:297–314
    [Google Scholar]
  123. 123.
    Sheldon RA. 2020. Catalytic oxidations in a bio-based economy. Front. Chem. 8:132
    [Google Scholar]
  124. 124.
    Shen G, Canniffe DP, Ho MY, Kurashov V, van der Est A et al. 2019. Characterization of chlorophyll f synthase heterologously produced in Synechococcus sp. PCC 7002. Photosynth. Res. 140:77–92
    [Google Scholar]
  125. 125.
    Sheridan KJ, Duncan EJ, Eaton-Rye JJ, Summerfield TC. 2020. The diversity and distribution of D1 proteins in cyanobacteria. Photosynth. Res. 145:111–28
    [Google Scholar]
  126. 126.
    Shi T, Bibby TS, Jiang L, Irwin AJ, Falkowski PG. 2005. Protein interactions limit the rate of evolution of photosynthetic genes in cyanobacteria. Mol. Biol. Evol. 22:2179–89
    [Google Scholar]
  127. 127.
    Shih PM, Hemp J, Ward LM, Matzke NJ, Fischer WW. 2017. Crown group Oxyphotobacteria postdate the rise of oxygen. Geobiology 15:19–29
    [Google Scholar]
  128. 128.
    Sicora CI, Chis I, Chis C, Sicora O. 2019. Regulation of PSII function in Cyanothece sp. ATCC 51142 during a light-dark cycle. Photosynth. Res. 139:461–73
    [Google Scholar]
  129. 129.
    Sicora CI, Ho FM, Salminen T, Styring S, Aro EM. 2009. Transcription of a “silent” cyanobacterial psbA gene is induced by microaerobic conditions. Biochim. Biophys. Acta Bioenerg. 1787:105–12
    [Google Scholar]
  130. 130.
    Ślesak I, Ślesak H, Kruk J. 2012. Oxygen and hydrogen peroxide in the early evolution of life on Earth: in silico comparative analysis of biochemical pathways. Astrobiology 12:775–84
    [Google Scholar]
  131. 131.
    Slotznick SP, Johnson JE, Rasmussen B, Raub TD, Webb SM et al. 2022. Reexamination of 2.5-Ga “whiff” of oxygen interval points to anoxic ocean before GOE. Sci. Adv. 8:eabj7190
    [Google Scholar]
  132. 132.
    Soo RM, Hemp J, Hugenholtz P. 2019. Evolution of photosynthesis and aerobic respiration in the cyanobacteria. Free Radical Biol. Med. 140:200–5
    [Google Scholar]
  133. 133.
    Soo RM, Woodcroft BJ, Parks DH, Tyson GW, Hugenholtz P. 2015. Back from the dead; the curious tale of the predatory cyanobacterium Vampirovibrio chlorellavorus. PeerJ 3:e968
    [Google Scholar]
  134. 134.
    Sugiura M, Azami C, Koyama K, Rutherford AW, Rappaport F, Boussac A. 2013. Modification of the pheophytin redox potential in Thermosynechococcus elongatus Photosystem II with PsbA3 as D1. Biochim. Biophys. Acta Bioenerg. 1837:139–48
    [Google Scholar]
  135. 135.
    Sugiura M, Boussac A. 2014. Some Photosystem II properties depending on the D1 protein variants in Thermosynechococcus elongatus. Biochim. Biophys. Acta Bioenerg. 1837:1427–34
    [Google Scholar]
  136. 136.
    Sugiura M, Ogami S, Kusumi M, Un S, Rappaport F, Boussac A. 2012. Environment of TyrZ in photosystem II from Thermosynechococcus elongatus in which PsbA2 is the D1 protein. J. Biol. Chem. 287:13336–47
    [Google Scholar]
  137. 137.
    Summerfield TC, Toepel J, Sherman LA. 2008. Low-oxygen induction of normally cryptic psbA genes in cyanobacteria. Biochemistry 47:12939–41
    [Google Scholar]
  138. 138.
    Tan C, Xu P, Tao F. 2022. Carbon-negative synthetic biology: challenges and emerging trends of cyanobacterial technology. Trends Biotechnol. 40:1488–502
    [Google Scholar]
  139. 139.
    Toepel J, Welsh E, Summerfield TC, Pakrasi HB, Sherman LA. 2008. Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth. J. Bacteriol. 190:3904–13
    [Google Scholar]
  140. 140.
    Trinugroho JP, Beckova M, Shao SX, Yu JF, Zhao ZY et al. 2020. Chlorophyll f synthesis by a super-rogue photosystem II complex. Nat. Plants 6238–44Characterization of a photosystem II complex with catalysis beyond water oxidation.
  141. 141.
    Utami YD, Kuwahara H, Igai K, Murakami T, Sugaya K et al. 2019. Genome analyses of uncultured TG2/ZB3 bacteria in ‘Margulisbacteria’ specifically attached to ectosymbiotic spirochetes of protists in the termite gut. ISME J. 13:455–67
    [Google Scholar]
  142. 142.
    van Niel CB. 1949. The comparative biochemistry of photosynthesis. Am. Sci. 37:371–83
    [Google Scholar]
  143. 143.
    van Niel CB. 1956. Evolution as viewed by the microbiologist. The Microbe's Contribution to Biology AJ Kluyver CB van Niel155–76. Cambridge, MA: Harvard Univ. Press
    [Google Scholar]
  144. 144.
    Vermaas WF. 1994. Evolution of heliobacteria: implications for photosynthetic reaction center complexes. Photosynth. Res. 41:285–94
    [Google Scholar]
  145. 145.
    Vinyard DJ, Gimpel J, Ananyev GM, Mayfield SP, Dismukes GC. 2014. Engineered Photosystem II reaction centers optimize photochemistry versus photoprotection at different solar intensities. J. Am. Chem. Soc. 136:4048–55
    [Google Scholar]
  146. 146.
    Wahart AJC, Staniland J, Miller GJ, Cosgrove SC. 2022. Oxidase enzymes as sustainable oxidation catalysts. R. Soc. Open Sci. 9:211572
    [Google Scholar]
  147. 147.
    Walker JCG. 1980. Atmospheric constraints on the evolution of metabolism. Orig. Life 10:93–104
    [Google Scholar]
  148. 148.
    Wang XL, Planavsky NJ, Hofmann A, Saupe EE, De Corte BP et al. 2018. A Mesoarchean shift in uranium isotope systematics. Geochim. Cosmochim. Acta 238:438–52
    [Google Scholar]
  149. 149.
    Wegener KM, Nagarajan A, Pakrasi HB. 2015. An atypical psbA gene encodes a sentinel D1 protein to form a physiologically relevant inactive photosystem II complex in cyanobacteria. J. Biol. Chem. 290:3764–74
    [Google Scholar]
  150. 150.
    Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M et al. 2016. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1:16116
    [Google Scholar]
  151. 151.
    Williams JC, Steiner LA, Ogden RC, Simon MI, Feher G. 1983. Primary structure of the M subunit of the reaction center from Rhodopseudomonas sphaeroides. PNAS 80:6505–9
    [Google Scholar]
  152. 152.
    Wisecaver JH, Hackett JD. 2011. Dinoflagellate genome evolution. Annu. Rev. Microbiol. 65:369–87
    [Google Scholar]
  153. 153.
    Wohlgemuth R, Twardowski T, Aguilar A. 2021. Bioeconomy moving forward step by step—a global journey. N. Biotechnol. 61:22–28
    [Google Scholar]
  154. 154.
    Wu A, Hammer GL, Doherty A, von Caemmerer S, Farquhar GD. 2019. Quantifying impacts of enhancing photosynthesis on crop yield. Nat. Plants 5:380–88
    [Google Scholar]
  155. 155.
    Xiao Y, Huang G, You X, Zhu Q, Wang W et al. 2021. Structural insights into cyanobacterial photosystem II intermediates associated with Psb28 and Tsl0063. Nat. Plants 7:1132–42
    [Google Scholar]
  156. 156.
    Xiong J, Bauer CE. 2002. A cytochrome b origin of photosynthetic reaction centers: an evolutionary link between respiration and photosynthesis. J. Mol. Biol. 322:1025–37
    [Google Scholar]
  157. 157.
    Yang Y, Arnold FH. 2021. Navigating the unnatural reaction space: directed evolution of heme proteins for selective carbene and nitrene transfer. Acc. Chem. Res. 54:1209–25
    [Google Scholar]
  158. 158.
    Yao DCI, Brune DC, Vermaas WFJ. 2012. Lifetimes of photosystem I and II proteins in the cyanobacterium Synechocystis sp. PCC 6803. FEBS Lett. 586:169–73
    [Google Scholar]
  159. 159.
    Zabret J, Bohn S, Schuller SK, Arnolds O, Möller M et al. 2021. Structural insights into photosystem II assembly. Nat. Plants 7:524–38
    [Google Scholar]
  160. 160.
    Zamocky M, Janecek S, Koller F. 2000. Common phylogeny of catalase-peroxidases and ascorbate peroxidases. Gene 256:169–82
    [Google Scholar]
  161. 161.
    Zeymer C, Hilvert D. 2018. Directed evolution of protein catalysts. Annu. Rev. Biochem. 87:131–57
    [Google Scholar]
  162. 162.
    Zhang G-J, Dong R, Lan L-N, Li S-F, Gao W-J, Niu H-X. 2020. Nuclear integrants of organellar DNA contribute to genome structure and evolution in plants. Int. J. Mol. Sci. 21:707
    [Google Scholar]
  163. 163.
    Zhang Z, Green BR, Cavalier-Smith T. 2000. Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: a possible common origin for sporozoan and dinoflagellate plastids. J. Mol. Evol. 51:26–40
    [Google Scholar]
  164. 164.
    Zimmerman JB, Anastas PT, Erythropel HC, Leitner W. 2020. Designing for a green chemistry future. Science 367:397–400
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-070522-062509
Loading
/content/journals/10.1146/annurev-arplant-070522-062509
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error