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Moving to the Light: The Evolution of Photosynthesis

  • Roberto Ligrone
Chapter

Abstract

Photosynthesis enabled early life to severe its ancestral dependence on geochemistry. The paleogeochemical record suggests that photosynthetic life colonized the planet photic zone as early as 3.4 GYA. Photosynthesis evolved in the Bacteria domain, and initially utilized compounds of geochemical origin such as ferrous iron or hydrogen as sources of electrons, without producing oxygen. Several variants of anoxygenic photosynthesis are present in extant bacteria. The cyanobacteria evolved oxygenic photosynthesis, a pathway that deploys two types of photosystem working in series to sum the energy of two photons for each electron transported from water to carbon dioxide. Multiple sources of evidence suggest that the cyanobacteria and oxygenic photosynthesis appeared at least 2.7 GYA, viz. 300 MY before the stable oxygenation of the planet. Endosymbiosis horizontally transferred oxygenic photosynthesis to the eukaryotes. Major similarities in the molecular architecture of photosystems in extant bacterial lineages point to a monophyletic origin of the core photosynthetic machine, followed by horizontal transfer among distantly related taxa, duplication and neo-functionalization. The Archaea lack photosynthesis but independently evolved a phototrophic pathway based on rhodopsins. Among a diversity of metabolic pathways for inorganic carbon fixation, the RubisCO-based Calvin, Benson and Bassham cycle is by far predominant.

References

  1. Allen JF et al (2011) A structural phylogenetic map for chloroplast photosynthesis. Trends Plant Sci 16:645–655PubMedCrossRefGoogle Scholar
  2. Anbar AD et al (2007) A whiff of oxygen before the great oxidation event? Science 317:1903–1906PubMedPubMedCentralCrossRefGoogle Scholar
  3. Barber J (2012) Photosystem II: the water-splitting enzyme of photosynthesis. Cold Spring Harb Symp Quant Biol 77:295–306.  https://doi.org/10.1101/sqb.2012.77.014472 PubMedCrossRefGoogle Scholar
  4. Beatty JT et al (2005) An obligately photosynthetic bacterial anaerobe from a deep-sea hydrothermal vent. Proc Natl Acad Sci U S A 102:9306–9310PubMedPubMedCentralCrossRefGoogle Scholar
  5. Béjà O et al (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289:1902–1906PubMedPubMedCentralCrossRefGoogle Scholar
  6. Béjà O et al (2001) Proteorhodopsin phototrophy in the ocean. Nature 411:786–789PubMedCrossRefGoogle Scholar
  7. Bekker A et al (2010) Iron formation: the sedimentary product of a complex interplay among mantle, tectonic, oceanic, and biospheric processes. Econ Geol 105:467–508CrossRefGoogle Scholar
  8. Blankenship RE (2010) Early evolution of photosynthesis. Plant Physiol 154:434–438PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bosak T et al (2009) Morphological record of oxygenic photosynthesis in conical stromatolites. Proc Natl Acad Sci U S A 106:10939–10943PubMedPubMedCentralCrossRefGoogle Scholar
  10. Brasier M et al (2006) A fresh look at the fossil evidence for early Archaean cellular life. Philos Trans R Soc B 361:887–902CrossRefGoogle Scholar
  11. Brocks JJ et al (2003) A reconstruction of Archean biological diversity based on molecular fossils from the 2.78 to 2.45 billion-year-old Mount Bruce Supergroup, Hamersley Basin, Western Australia. Geochim Cosmochim Acta 67:4321–4335CrossRefGoogle Scholar
  12. Bryant DA (2007) Candidatus Chloracidobacterium thermophilum: an aerobic phototrophic acidobacterium. Science 317:523–526PubMedCrossRefGoogle Scholar
  13. Bryant DA, Frigaard N-U (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends Microbiol 14:488–496PubMedCrossRefGoogle Scholar
  14. Buick R (2008) When did oxygenic photosynthesis evolve? Philos Trans R Soc B 363:2731–2743CrossRefGoogle Scholar
  15. Butterfield NJ (2015) Proterozoic photosynthesis – a critical review. Palaeontology 58:95–972.  https://doi.org/10.1111/pala.12211 CrossRefGoogle Scholar
  16. Crowe S et al (2013) Atmospheric oxygenation three billion years ago. Nature 501:535–538PubMedCrossRefGoogle Scholar
  17. David LA, Alm EJ (2011) Rapid evolutionary innovation during an Archaean genetic expansion. Nature 469:93–96PubMedCrossRefGoogle Scholar
  18. Dismukes GC et al (2001) The origin of atmospheric oxygen on Earth: the innovation of oxygenic photosynthesis. Proc Natl Acad Sci U S A 98:2170–2175PubMedPubMedCentralCrossRefGoogle Scholar
  19. French KL et al (2015) Reappraisal of hydrocarbon biomarkers in Archean rocks. Proc Natl Acad Sci U S A 112:5915–5920PubMedPubMedCentralCrossRefGoogle Scholar
  20. Fuchs G (2011) Alternative pathways of carbon dioxide fixation: insights into the early evolution of life? Annu Rev Microbiol 65:631–658PubMedCrossRefGoogle Scholar
  21. Gupta RS (2012) Origin and spread of photosynthesis based upon conserved sequence features in key bacteriochlorophyll biosynthesis proteins. Mol Biol Evol 29:3397–3412PubMedCrossRefGoogle Scholar
  22. Gutteridge S, Pierce J (2006) A unified theory for the basis of the limitations of the primary reaction of photosynthetic CO2 fixation: was Dr. Pangloss right? Proc Natl Acad Sci U S A 103:7203–7204PubMedPubMedCentralCrossRefGoogle Scholar
  23. Hohmann-Marriott MF, Blankenship RE (2011) Evolution of photosynthesis. Annu Rev Plant Biol 62:515–548PubMedCrossRefGoogle Scholar
  24. Hoshino Y et al (2015) Hydrocarbons preserved in a ~2.7 Ga outcrop sample from the Fortescue Group, Pilbara Craton, Western Australia. Geobiology 13:99–111PubMedCrossRefGoogle Scholar
  25. Kirschvink JL, Kopp RE (2008) Paleoproterozoic ice houses and the evolution of oxygen-mediating enzymes: the case for a late origin of photosystem II. Philos Trans R Soc B 363:2755–2765CrossRefGoogle Scholar
  26. Li W, Beard BL, Johnson CM (2015) Biologically recycled continental iron is a major component in banded iron formations. Proc Natl Acad Sci U S A 112:8193–8198PubMedPubMedCentralCrossRefGoogle Scholar
  27. Lyons TW, Reinhard CT, Planavsky NJ (2014) The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506:307–315PubMedCrossRefGoogle Scholar
  28. Mukhopadhyay J et al (2014) Oxygenation of the Archean atmosphere: new paleosol constraints from eastern India. Geology 42:923–926CrossRefGoogle Scholar
  29. Muller E et al (2017) Primary sulfur isotope signatures preserved in high-grade Archean barite deposits of the Sargur Group, Dharwar Craton, India. Precambrian Res 295:38–47CrossRefGoogle Scholar
  30. Nelson N, Junge W (2015) Structure and energy transfer in photosystems of oxygenic photosynthesis. Annu Rev Biochem 84:659–683PubMedCrossRefGoogle Scholar
  31. Nisbet EG et al (2007) The age of Rubisco: the evolution of oxygenic photosynthesis. Geobiology 5:311–335CrossRefGoogle Scholar
  32. Ohtomo Y et al (2013) Evidence for biogenic graphite in early Archean Isua metasedimentary rocks. Nat Geosci 7:25–28CrossRefGoogle Scholar
  33. Olson JM (2006) Photosynthesis in the Archaean era. Photosynth Res 88:109–117PubMedCrossRefGoogle Scholar
  34. Perez N et al (2013) The potential for photosynthesis in hydrothermal vents: a new avenue for life in the Universe? Astrophys Space Sci 346:327–331CrossRefGoogle Scholar
  35. Planavsky NJ et al (2014) Evidence for oxygenic photosynthesis half a billion years before the Great Oxidation Event. Nat Geosci 7:283–286CrossRefGoogle Scholar
  36. Rasmussen B et al (2008) Reassessing the first appearance of eukaryotes and cyanobacteria. Nature 455:1101–1104PubMedCrossRefGoogle Scholar
  37. Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos Trans R Soc B 363:2641–2650CrossRefGoogle Scholar
  38. Raymond J et al (2003) Evolution of photosynthetic prokaryotes: a maximum-likelihood mapping approach. Philos Trans R Soc B 358:223–230CrossRefGoogle Scholar
  39. Renzaglia KS et al (2007) Bryophyte phylogeny: advancing the molecular and morphological frontiers. Bryologist 110:179–213CrossRefGoogle Scholar
  40. Řezanka T et al (2010) Hopanoids in bacteria and cyanobacteria – their role in cellular biochemistry and physiology, analysis and occurrence. Mini-Rev Org Chem 7:300–313CrossRefGoogle Scholar
  41. Ricci JN, Michel AJ, Newman DK (2015) Phylogenetic analysis of HpnP reveals the origin of 2-methylhopanoid production in Alphaproteobacteria. Geobiology 13:267–277PubMedCrossRefGoogle Scholar
  42. Rosing MT (1999) 13C-depleted carbon microparticles in 3700 Ma sea-floor sedimentary rocks from West Greenland. Science 283:674–676PubMedCrossRefGoogle Scholar
  43. Rothschild LJ (2008) The evolution of photosynthesis…again. Philos Trans R Soc B 363:2787–2801CrossRefGoogle Scholar
  44. Schirrmeister BE et al (2013) Evolution of multicellularity coincided with increased diversification of cyanobacteria and the Great Oxidation Event. Proc Natl Acad Sci U S A 110:1791–1796PubMedPubMedCentralCrossRefGoogle Scholar
  45. Schirrmeister BE, Gugger M, Donoghue PCJ (2015) Cyanobacteria and the Great Oxidation Event: evidence from genes and fossils. Palaeontology 58:769–785PubMedPubMedCentralCrossRefGoogle Scholar
  46. Schopf JW (2006) Fossil evidence of Archean life. Philos Trans R Soc B 361:869–885CrossRefGoogle Scholar
  47. Schopf JW et al (2017) An anaerobic ∼3400 Ma shallow-water microbial consortium: presumptive evidence of Earth’s Paleoarchean anoxic atmosphere. Precambrian Res 299:309–318CrossRefGoogle Scholar
  48. Sugitani K et al (2015) Early evolution of large micro-organisms with cytological complexity revealed by microanalyses of 3.4 Ga organic-walled microfossils. Geobiology 13:507–521PubMedCrossRefGoogle Scholar
  49. Tabita FR (2009) The hydroxypropionate pathway of CO2 fixation: fait accompli. Proc Natl Acad Sci 106:21015–21016PubMedCrossRefGoogle Scholar
  50. Tabita FR et al (2008) Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Philos Trans R Soc B 363:2629–2640CrossRefGoogle Scholar
  51. Tcherkez GGB, Farquhar GD, Andrews TJ (2006) Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proc Natl Acad Sci U S A 103:7246–7251PubMedPubMedCentralCrossRefGoogle Scholar
  52. Vermaas WFJ (2002) Photosynthesis and respiration in cyanobacteria. Encycl Life Sci.  https://doi.org/10.1038/npg.els.0001670
  53. Waldbauer JR et al (2009) Late Archean molecular fossils from the Transvaal Supergroup record the antiquity of microbial diversity and aerobiosis. Precambrian Res 169:28–47CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Roberto Ligrone
    • 1
  1. 1.Department of Environmental, Biological and Pharmaceutical Sciences and TechnologiesUniversity of Campania “Luigi Vanvitelli”CasertaItaly

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