Photosynthetica

, Volume 56, Issue 1, pp 11–43 | Cite as

Living off the Sun: chlorophylls, bacteriochlorophylls and rhodopsins

Review

Abstract

Pigments absorbing 350–1,050 nm radiation have had an important role on the Earth for at least 3.5 billion years. The ion pumping rhodopsins absorb blue and green photons using retinal and pump ions across cell membranes. Bacteriochlorophylls (BChl), absorbing in the violet/blue and near infra red (NIR), power anoxygenic photosynthesis, with one photoreaction centre; and chlorophylls (Chl), absorbing in the violet/blue and red (occasionally NIR) power oxygenic photosynthesis, with two photoreaction centres. The accessory (bacterio)chlorophylls add to the spectral range (bandwidth) of photon absorption, e.g., in algae living at depth in clear oceanic water and in algae and photosynthetic (PS) bacteria in microbial mats. Organism size, via the package effect, determines the photon absorption benefit of the costs of synthesis of the pigment–protein complexes. There are unresolved issues as to the evolution of Chls vs. BChls and the role of violet/blue and NIR radiation in PS bacteria.

Abbreviations

AAPB

aerobic anoxygenic aerobic photosynthesis

BChl

bacteriochlorophyll

Chl

chlorophyll

ETR

electron transport rate

GOE

Great Oxidation Event

HPLC

high performance liquid chromatography

LED

light-emitting diode

LGT

lateral gene transfer

MgDVP

magnesium-2,4-divinyl phaeoporphyrin monomethyl ester A5

PBP

phycobiliprotein

RC

reaction center

TLC

thin layer chromatography

UV

ultraviolet

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References

  1. Agusti S., Phlips E.J.: Light absorption by cyanobacteria: implications of the colonial growth form.–Limnol. Oceanogr. 37: 434–441, 1992.Google Scholar
  2. Akimoto S., Shinoda T., Chen M. et al.: Energy transfer in the chlorophyll f-containing cyanobacterium, Halomicronema hongdechloris, analyzed by time-resolved fluorescence spectroscopies–Photosynth. Res. 125: 115–122, 2015.PubMedGoogle Scholar
  3. Albarracín V.H., Kraiselburd I., Bamann C. et al.: Functional green-tuned proteorhodopsin from modern stromatolites.–PLoS ONE 11: e0154962, 2016.PubMedPubMedCentralGoogle Scholar
  4. Allakhverdiev S.I., Kreslavski V.D., Zharmukhamedov S.K.: Chlorophylls d and f and their role in primary photodynthetic processes of cyanobacteria.–Biochemistry-Moscow 81: 201–212, 2016.PubMedGoogle Scholar
  5. Allen M.B.: Distribution of the chorophylls.–In: Vernon L.P., Seeley G.R. (ed.): The Chlorophylls: Physical, Chemical and Biological Properties. Pp. 511–519. Academic Press, New York and London 1996.Google Scholar
  6. Aronoff S.: The chlorophylls–an introductory survey.–In: Vernon L.P., Seeley G.R. (ed.): The Chlorophylls: Physical, Chemical and Biological Properties. Pp. 3–20. Academic Press, New York and London 1966.Google Scholar
  7. Atamna-Ismaeel N., Finkel O.M., Glaser F. et al.: Microbial rhodopsins on leaf surfaces of terrestrial plants.–Environ. Microbiol. 14: 140–146, 2012.PubMedGoogle Scholar
  8. Atamna-Ismaeel N., Sabehi G., Sharon I. et al.: Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems.–ISME J. 2: 656–662, 2008.PubMedGoogle Scholar
  9. Bamberg E., Tittor J., Oesterhelt D.: Light-driven proton or chloride pumping by halorhodopsin.–P. Natl. Acad. Sci. USA 90: 639–643, 1993.Google Scholar
  10. Battistuzzi F.U., Feijao A., Hedges S.B.: A genomic timescale of prokaryote evolution: insights into the origin of methanogenesis, phototrophy, and the colonization of land.–BMC Evol. Biol. 4: 44, 2004.PubMedPubMedCentralGoogle Scholar
  11. Battistuzzi F.U., Hedges S.B.: A major clade of prokaryotes with ancient adaptations to life on land.–Mol. Biol. Evol. 26: 335–343, 2009.PubMedGoogle Scholar
  12. Baumann C., Bamberg E., Waxhveitl J.: Proteorhodopsin.–Biochim. Biophys. Acta 1837: 614–625, 2014.Google Scholar
  13. Beardall J., Allen D., Bragg J.: Allometry and stoichometry of unicellular, colonial and multicellular phytoplankton.–New Phytol. 181: 295–309, 2009.PubMedGoogle Scholar
  14. Beer-Romero P., Gest H.: Heliobacillus mobilis, a peritrichously flagellated anoxyphototroph containing bacteriochlorophyll g.–FEMS Microbiol. Lett. 41: 109–114, 1987.Google Scholar
  15. Behrendt L., Brejnrod A., Schliep M. et al.: Chlorophyll f-driven photosynthesis in a cavernous cyanobacterium.–ISME J. 9: 2108–2111, 2015.PubMedPubMedCentralGoogle Scholar
  16. Béjà O., Spudich E.N., Spudich J.L. et al.: Proteorhodopsin phototrophy in the ocean.–Nature 411: 786–789, 2001.PubMedGoogle Scholar
  17. Beraldi-Campesi H.: Early life on land and the first terrestrial ecosystems.–Ecol. Process. 2: 1, 2013.Google Scholar
  18. Bieliwski J.P., Dunn K.A., Sabehi G. et al.: Darwinian adaptation of proteorhodopsin to different light intensities in the marine environment.–P. Natl. Acad. Sci. USA 101: 14824–14829, 2004.Google Scholar
  19. Bína D., Gardian Z., Herbstová M. et al.: Novel type of redshifted chlorophyll a antenna complex from Chromera velia II. Biochemistry and spectroscopy.–BBA-Bioenergetics 1837: 802–810, 2014.PubMedGoogle Scholar
  20. Binzer T., Sand-Jensen K.: Importance of structure and density of macroalgae communities (Fucus serratus) for photosynthetic production and light utilisation.–Mar. Ecol. Prog. Ser. 235: 53–62, 2002Google Scholar
  21. Björn L.O., Papageorgiou G.C., Blankenship R.F. et al.: A viewpoint: why chlorophyll a?–Photosynth. Res. 99: 85–98, 2009.PubMedGoogle Scholar
  22. Björn L.O.: Why are plants green–relationships between pigment absorption and photosynthetic efficiency.–Photosynthetica 10: 121–129, 1976.Google Scholar
  23. Blank C.E., Sánchez-Baracaldo P.: Timing of morphological and ecological innovations in the cyanobacteria–a key to understanding the rise in atmospheric oxygen.–Geobiology 8: 1–23, 2010.PubMedGoogle Scholar
  24. Blankenship R.E., Madigan M.T., Bauer C.E. (ed.): Anoxygenic Photosynthetic Bacteria. Pp. 1331. Kluwer Academic Publications, Dordrecht–Boston–London 1995.Google Scholar
  25. Blankenship R.E., Tiede D.M., Barber J. et al.: Comparing photosynthetic and photovoltaic efficiencies and recognising the potential for improvement.–Science 332: 805–809, 2011.PubMedGoogle Scholar
  26. Bogachev A.V., Bertsova Y.V., Verkhovsakaya M.L. et al.: Real-time kinetics of electrogenic Na+ transport by rhodopsin from the marine flavobacterium Dokdonia sp. PRO95.–Sci. Rep. 6: 21397, 2016.PubMedPubMedCentralGoogle Scholar
  27. Boichenko V.A., Pinevich A.V., Stadnichuk I.N.: Association of chlorophyll a/b-binding Pcb proteins with photosystems I and II in Prochlorothrix hollandica.–BBA-Bioenergetics 1767: 801–806, 2007.PubMedGoogle Scholar
  28. Borra C., Brunett C. et al.: Phylogenetic position of Crustomastix stigmata, sp.nov., and Dolichmastix tenuilepis in relation to the Mamiellaes (Prasiophyceae, Chlorophyta).–J. Phycol. 38: 1024–1039, 2002Google Scholar
  29. Bowmaker J.K., Dartnall H.J.: Visual pigments of rods and cones in a human retina.–J. Physiol. 298: 501–511, 1980.PubMedPubMedCentralGoogle Scholar
  30. Brindefalk B., Ekman M., Ininbergs K. et al.: Distribution and expression of microbial rhodopsins in Baltic Sea and adjacent waters.–Environ. Microbiol. 18: 4442–4455, 2016.PubMedGoogle Scholar
  31. Brockmann H. Jr., Lipinski A.: Bacteriochlorophyll g. A new bacteriochlorophyll from Heliobacterium chlorum.–Arch. Microbiol. 136: 17–19, 1983.Google Scholar
  32. Bryant D.B., Frigaard N.-U.: Prokaryotic photosynthesis and phototrophy illuminated.–Trends Microbiol. 14: 488–496, 2006.PubMedGoogle Scholar
  33. Buitenhuis E.T., Hasioka T., Le Quéré R.: Combined constraints on global ocean production using observations and models.–Glob. Change Biol. 27: 847–858, 2013.Google Scholar
  34. Bumba L. Prášil O., Vácha F.: Antenna ring around trimeric photosystem I in chlorophyll b containing cyanobacterium Prochlorothrix hollandica.–BBA-Bioenergetics 1708: 1–5, 2005.PubMedGoogle Scholar
  35. Burke D.H., Alberti M., Hearst J.E.: bchFNBH bacteriochlorophyll synthesis genes of Rhodobacter capsulatus and identification of the third subunit of light-independent protochlorophyllide reductase in bacteria and plants.–J. Bacteriol. 175: 2414–2422, 1993.PubMedPubMedCentralGoogle Scholar
  36. Burns B.P, Goh F., Allen M., Neilan B.A.: Microbial diversity of extant stromatolites in thehypersaline marine environment of Shark Bay, Australia.–Environ. Microbiol. 6: 1096–1101, 2004.PubMedGoogle Scholar
  37. Butterfield N.J.: Proterozoic photosynthesis–a critical review.–Paleontology 58: 953–972, 2015.Google Scholar
  38. Cardona T.: Reconstructing the origin of oxygenic photosynthesis: Do assembly and photoactivation recapitulate evolution?–Front. Plant Sci. 7: 257, 2016.PubMedPubMedCentralGoogle Scholar
  39. Chen M.: Chlorophyll modifications and their spectral extension in oxygenic photosynthesis.–Annu. Rev. Biochem. 83: 317–340, 2014.PubMedGoogle Scholar
  40. Chen M., Blankenship R.E.: Expanding the solar spectrum used by photosynthesis.–Trends Plant Sci. 16: 427–431, 2011.PubMedGoogle Scholar
  41. Chen M., Eggink L., Hoober J.K. et al.: Influence of structure on binding of chlorophylls to peptide ligands.–J. Am. Chem. Soc. 127: 2052–2053, 2005.PubMedGoogle Scholar
  42. Chen M., Hiller R.H., Howe C.J. et al.: Unique origin and lateral transfer of prokaryotic chlorophyll b and chlorophyll d lightharvesting systems.–Mol. Biol. Evol. 22: 21–28, 2005.PubMedGoogle Scholar
  43. Chen M., Schliep M., Willows R. et al.: A red-shifted chlorophyll.–Science 329: 1318–1319, 2010.PubMedGoogle Scholar
  44. Chen M., Li Y., Birch D., Willows R.D.: A cyanobacterium that contains chlorophyll f–a red-absorbing photopigment.–FEBS Lett. 586: 3249–3254, 2012.PubMedGoogle Scholar
  45. Chen M., Scheer H.: Extending the limits of natural photosynthesis and implications for technical light harvesting.–J. Porphyr. Phthalocyan. 17: 1–15, 2013.Google Scholar
  46. Chisholm S.W., Frankel S.L., Goericke R. et al.: Prochlorococcus-marinus nov. gen. nov. sp.–an oxyphototrophic marine prokaryote containing divinyl chlorophyll-a and chlorophyll-b.–Arch. Microbiol. 157: 297–300, 1992.Google Scholar
  47. Choi A.R., Shi L., Brown L.S. et al.: Cyanobacterial light-driven proton pump, Gloeobacter rhodopsin: complementarity between rhodopsin-based energy production and photosynthesis.–PLoS ONE 9: e110643, 2014.PubMedPubMedCentralGoogle Scholar
  48. Claire M.W., Sheets J., Cohen M. et al.: The evolution of solar flux from 0.1 nm to 160 μm: quantitative estimates for planetary studies.–Astrophys. J. 757: 95, 2012.Google Scholar
  49. Cockell C.S., Kaltenegger L., Raven J.A.: Cryptic photosynthesis–extrasolar planetary oxygen without a surface biological signature.–Astrobiology 9: 623–636, 2009.PubMedGoogle Scholar
  50. Cockell C.S., Raven J.A.: Ozone and life on the Archaean Earth.–Philos. T. Roy. Soc. A 365: 1889–1907, 2008.Google Scholar
  51. Courties A., Riedel T., Rapaport A. et al.: Light-driven increase in carbon yield is linked to maintenance in the proteobacterium Photobacterium angustum S14.–Front. Microbiol. 6: 688, 2015.PubMedPubMedCentralGoogle Scholar
  52. Crossett R.N., Drew E.A., Larkum A.W.D.: Chromatic adaptation in benthic marine algae.–Nature 207: 547–548, 1965.Google Scholar
  53. Dring M.J.: Chromatic adaptation of photosynthesis in benthic marine algae: an examination of its ecological significance using a theoretical model.–Limnol. Oceanogr. 26: 271–284, 1981.Google Scholar
  54. Durako M.J.: Leaf optical properties and photosynthetic leaf absorptances in several Australian seagrasses.–Aquat. Bot. 87: 83–89, 2007.Google Scholar
  55. Duysens L.N.M.: The flattening of absorption spectrum of suspensions, compared to that of solutes.–Biochim. Biophys. Acta 19: 1–12, 1956.PubMedGoogle Scholar
  56. Edwards D., Cherns L., Raven J.A.: Could land-based early photosynthesis ing ecosystems have bioengineered the planet in mid-Palaeozoic times?–Palaeontology 58: 803–837, 2015.Google Scholar
  57. Engqvist M.K.M., McIsaac R.S., Dollinger P. et al.: Directed evolution of Gloeobacter violaceous rhodopsin spectral properties.–J. Mol. Biol. 427: 205–220, 2015.PubMedGoogle Scholar
  58. Enríquez S., Agustí S., Duarte C.M.: Light Absorption by marine macrophytes.–Oecologia 98: 121–129, 1994.PubMedGoogle Scholar
  59. Falkowski P.G., Dubinsky Z., Wyman K.: Growth-irradiance relationships in phytoplankton.–Limnol. Oceanogr. 30: 311–321, 1985.Google Scholar
  60. Falkowski P.G., Raven J.A.: Aquatic Photosynthesis, 2nd Ed. Pp. 481. Princeton University Press, Princeton 2007.Google Scholar
  61. Fawley M.W.: Photosynthetic pigments of Pseudoscourfieldia marina and select green flagellates and coccoid ultraphytoplankton: implications for the systematics of the Micromonadophyceae (Chlorophyta).–J. Phycol. 28: 26–31, 1992.Google Scholar
  62. Feng S., Powell S.M., Wilson R. et al.: Light-stimulated growth of proteorhodopsin-bearing psychrophilic Psychoflexus torquis is salinity dependent.–ISME J. 7: 2206–2213, 2013.PubMedPubMedCentralGoogle Scholar
  63. Feniouk B.A., Junge W.: Proton translocation and ATP synthesis by the FoF1–ATPase of purple bacteria.–In: Hunter N., Daldal F., Thurnauer M.C., Beatty J.T. (ed.): The Purple Phototrophic Bacteria. Pp. 475–493. Springer, Dordrecht 2009.Google Scholar
  64. Ferrera I., Sánchez O., Kolářová E. et al.: Light enhances the growth rates of natural populations of aerobic anoxygenic phototrophic bacteria.–ISME J. 11: 2391–2393, 2017.PubMedGoogle Scholar
  65. Field C.B., Behrenfeld M.J., Randerson J.T. et al.: Primary production of the biosphere: integrating terrestrial and oceanic components.–Science 281: 237–240, 1998.PubMedGoogle Scholar
  66. Finkel Z.V., Beardall J., Flynn K.J. et al.: Phytoplankton in a changing world: cell size and elemental stoichiometry.–J. Plankton Res. 32: 118–137, 2010.Google Scholar
  67. Fork D.C., Amesz J.: Action spectra and energy transfer in photosynthesis.–Annu. Rev. Plant Phys. 20: 305–328, 1969Google Scholar
  68. Fork D.C., Larkum A.W.D.: Light harvesting in the green alga Oestreobium sp., a coral symbiont adapted to extreme shade.–Mar. Biol. 103: 381–385, 1989.Google Scholar
  69. French C.S.: The quantum yield of hydrogen and carbon dioxide accumulation in purple bacteria.–J. Gen. Physiol. 20: 711–735, 1937.PubMedPubMedCentralGoogle Scholar
  70. Frigaard N.-U., Chew A.G.M., Li H. et al.: Chlorobium tepidum: insights into the structure, physiology, and metabolism of a green sulphur bacterium derived from the complete genome sequence.–Photosynth. Res. 78: 93–117, 2003.PubMedGoogle Scholar
  71. Frigaard N.-U., Larsen K.L., Cox R.P.: Spectrochromatography of photosynthetic pigments as a fingerprinting technique for microbial phototrophs.–FEMS Microbiol. Ecol. 20: 69–77, 1996.Google Scholar
  72. Frigaard N.-U., Martinez A., Mincer T.J. et al.: Proteorhodopsin lateral gene transfer between marine planktonic Bacteria and Archaea.–Nature 439: 847–850, 2006.PubMedGoogle Scholar
  73. Frost-Christensen H., Sand-Jensen K.: The quantum efficiency of photosynthesis in macroalgae and submerged angiosperms.–Oecologia 91: 377–384, 1992.PubMedGoogle Scholar
  74. Fuhrman J.A, Schwalbach M.S., Stingl U.: Proteorhodopsins: an array of physiological roles?–Nat. Rev. Microbiol. 6: 488–494, 2008.PubMedGoogle Scholar
  75. Fuchs B.M., Spring S., Teeling H. et al.: Characterisation of a marine gamma proteobacterium capable of aerobic anoxygenic photosynthesis.–P. Natl. Acad. Sci. USA 108: 2891–2896, 2007.Google Scholar
  76. Ganapathy S., Venselaar H., Chen Q. et al.: Retinal-based proton pumping in the near-infrared.–J. Am. Chem. Soc. 139: 2338–2344, 2017.PubMedPubMedCentralGoogle Scholar
  77. Gao K., Ai H.: Relationship of growth and photosynthesis with colony size in an edible cyanobacterium, Ge-Xian-Mi Nostoc (Cyanophyceae).–J. Phycol. 40: 523–526, 2004.Google Scholar
  78. Garcia-Chaves M.C., Cottrell M.T., Kirchman D.L. et al.: Singlecell activity of freshwater aerobic anoxygenic phototrophic bacteria and their contribution to biomass production.–ISME J. 10: 1579–1588, 2016.PubMedPubMedCentralGoogle Scholar
  79. Gaudana S.B., Zarzycki J., Moparthi V.K. et al.: Bioinformatic analysis of the distribution of inorganic carbon transports and prospective targets for bioengineering to increase Ci uptake by cyanobacteria.–Photosynth. Res. 126: 99–109, 2015.PubMedGoogle Scholar
  80. Gloag R.S., Ritchie R.J., Chen M. et al.: Chromatic photoacclimation, photosynthetic electron transport and oxygen evolution in the Chlorophyll d-containing oxyphotobacterium Acaryochloris marina Miyashita.–BBA-Bioenergetics 1767: 127–135, 2007PubMedGoogle Scholar
  81. Goericke R., Repeta D.J.: Chlorophylls a and b and divinyl chlorophylls a and b in the open subtropical North Atlantic Ocean.–Mar. Ecol. Prog. Ser. 101: 307–313, 1993.Google Scholar
  82. Goericke R., Repeta D.J.: The pigments of Prochlorococcus marinus: the presence of divinylchlorophyll a and b in a marine procaryote.–Limnol. Oceanogr. 37: 425–433, 1992.Google Scholar
  83. Gómez I., Huovinen P.: Morpho-functional patterns and zonation of South Chilean seaweeds: the importance of photosynthetic and bio-optical traits.–Mar. Ecol. Prog. Ser. 422: 77–91, 2011.Google Scholar
  84. Gómez-Consarnau L., Akram N., Lindell K. et al.: Proteorhodopsin phototrophy promotes survival of marine bacteria during starvation.–PLoS Biol. 8: e1000358, 2010.PubMedPubMedCentralGoogle Scholar
  85. Gómez-Consarnau L., González J.M., Coll-Lladó M. et al.: Light stimulates growth of proteorhodopsin-containing marine Flavobacteria.–Nature 445: 210–213, 2007.PubMedGoogle Scholar
  86. Gould S.J., Lewontin R.C.: The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptionist programme.–P. Roy. Soc. B-Biol Sci 205: 581–598, 1979.Google Scholar
  87. Govindjee R., Balashov S.P. Ebrey T.G.: Quantum efficiency of the photochemical cycle of bacteriorhodopsin.–Biophys. J. 58: 597–606, 1990.PubMedPubMedCentralGoogle Scholar
  88. Govindjee, Shevela D., Björn L.O.: The evolution of the Zscheme of photosynthesis: a perspective.–Photosynth. Res. 133: 5–15, 2017.PubMedGoogle Scholar
  89. Graham J.E., Wilcox L.W., Graham L.E. et al.: Algae. 3rd Edition. eBook; www.lijmpress.com/algae.html, 2016.Google Scholar
  90. Granick S.: Evolution of heme and chlorophyll.–In: Bryson C., Vogel H.J. (ed.): Evolving Genes and Proteins. Pp. 67–88. Academic Press, New York, 1965.Google Scholar
  91. Greene R.M., Gerard V.A.: Effects of high frequency light fluctuations on growth and photoacclimation of the red alga Chondrus crispus.–Mar. Biol. 105: 337–344, 1990.Google Scholar
  92. Guo Z., Zhang H., Lin S.: Light-promoted rhodopsin expression and starvation survival in the marine dinoflagllate Oxyrrhis marina.–PLoS ONE 9: e114941, 2014.PubMedPubMedCentralGoogle Scholar
  93. Harada J., Mizoguchi T., Tsukatani Y. et al.: A seventh bacterial chlorophyll driving a large light-harvesting antenna.–Sci. Rep-UK 2: 671, 2012.Google Scholar
  94. Harel A., Karkar S., Cheng S. et al.: Deciphering primordial cyanobacterial genome functions from protein network analysis.–Curr. Biol. 25: 628–634, 2015.PubMedGoogle Scholar
  95. Harvey W.H.: A Manual of the British Algae. Pp. 52. John van Voorst, London 1849.Google Scholar
  96. Havosi F.I.: Spectral relation of core pigments in goldfish.–J. Gen. Physiol. 68: 65–80, 1976.Google Scholar
  97. Haxo F.T., Blinks L.R.: Action spectra of marine algae.–J. Gen. Physiol. 33: 389–422, 1950.PubMedPubMedCentralGoogle Scholar
  98. Hegemann P., Oesterbelt D., Steiner M.: The photocycle of the chloride pump halorhodopsin. I: Azide-catalysed deprotonation of the chromophore is a side reaction of photocycle intermediates inactivating the pump.–EMBO J. 4: 2347–2350, 1985.PubMedPubMedCentralGoogle Scholar
  99. Hellingwerf K.J. de Vrij W., Konings W.N.: Wavelength dependence of energy transduction in Rhodopseudomonas sphaeroides: action spectrum for growth.–J. Bacteriol. 151: 534–541, 1982.PubMedPubMedCentralGoogle Scholar
  100. Herbstová M., Litvín R., Gardian Z. et al.: Localization of Pcb antenna complexes in the photosynthetic prokaryote Prochlorothrix hollandica.–BBA-Bioenergetics 1797: 89–97, 2010.PubMedGoogle Scholar
  101. Ho M., Gan F., Shen G. et al.: Far-red light photoacclimation (FaRLiP) in Synechococcus sp. PCC 7335: I. Regulation of FaRLiP gene expression.–Photosynth. Res. 131: 173–186, 2017.PubMedGoogle Scholar
  102. Ho M.-Y., Shen G., Canniffe D.P. et al.: Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II.–Science 353: 886–887, 2016.Google Scholar
  103. Hohmann-Marriott M.F., Blankenship R.E.: Evolution of photosynthesis.–Annu. Rev. Plant Biol. 62: 515–548, 2011.PubMedGoogle Scholar
  104. Hoogewerf G.J, Jung D.O., Madigan M.T.: Evidence for limited species diversity of bacteriochlorophyll b-containing purple non-sulphur anoxygenic phototrophs in freshwater habitats.–FEMS Microbiol. Lett. 218: 359–364, 2003.PubMedGoogle Scholar
  105. Horath T., Bachofen R.: Molecular characterisation of an endolithic microbial community in dolomite rock in the Central Alps (Switzerland).–Environ. Microbiol. 58: 290–306, 2009.Google Scholar
  106. Hubas C., Jesus B., Passarelli C. et al.: Tools providing new insight into coastal anoxygenic purple bacterial mats.–Res. Microbiol. 162: 858–868, 2011.PubMedGoogle Scholar
  107. Hughes J.L., Smith P., Pace R. et al.: Charge separation in photosystem II core complexes induced by 690-730nm excitation at 1.7 K.–BBA-Bioenergetics 1757: 841–851, 2006.PubMedGoogle Scholar
  108. Hunter C.N., Coomber S.A.: Cloning and oxygen-regulated expression of the bacteriochlorophyll biosynthesis genes bch,E, B, A and C of Rhodobacter spheroids.–J. Gen. Microbiol. 134: 1491–1497, 1988.Google Scholar
  109. Itoh S., Ohno T., Noji T. et al.: Harvesting far-red light by chlorophyll f in photosystems I and II of unicellular cyanobacterium strain KC1.–Plant Cell Physiol. 56: 2024–2034, 2015.PubMedGoogle Scholar
  110. Janke C., Scholz F., Becker-Baldus J. et al.: Photocycle and vectorial proton transfer in a rhodopsin from the eukaryote proton transfer in a rhodopsin from the eukaryote Oxyrrhis marina.–Biochemistry 52: 2750–2763, 2013.PubMedGoogle Scholar
  111. Jiao N., Zhang Y., Zeng Y. et al.: Distinct distribution pattern of abundance and diversity of aerobic anoxygenic phototrophic bacteria in the global ocean.–Environ. Microbiol. 9: 3091–3099, 2007.PubMedGoogle Scholar
  112. Johnston D.T., Wolfe-Simon F., Pearson A. et al.: Anxygenic photosynthesis modulated Proterozoic oxygen and sustained Earth’s middle age.–P. Natl. Acad. Sci. USA 106: 16925–16929, 2009.Google Scholar
  113. Jones H.G.: Plants and Microclimate. A Quantitative Approach to Environmental Plant Physiology. 3rd Edition. Pp. 527. Cambridge University Press, Cambridge 2013.Google Scholar
  114. Kaňa R., Prášil O., Mullineaux C.C.: Immobility of phycobilins in the thylakoid lumen of as cryptophyte suggests that protein diffusion in the lumen is very restricted.–FEBS Lett. 583: 670–674, 2009.PubMedGoogle Scholar
  115. Kandori H.: Ion-pumping microbial rhodopsins.–Front. Mol. Biosci. 2: 52, 2015.PubMedPubMedCentralGoogle Scholar
  116. Kang I., Oh H.M., Lim S.I. et al.: Genome sequence of Fulvimarina pelagi HTCC2506(T), a Mn(II)-oxidising alphaproteobacterium possessing an aerobic anoxygenic photosynthetic gene cluster and xanthorhodopsin.–J. Bacteriol. 192: 4798–4799, 2010.PubMedPubMedCentralGoogle Scholar
  117. Kantz T.S., Theriot E.C., Zimmer E.A. et al.: The Pleurastrophyceae and Micromonadophyceae: a cladistic analysis of nuclear ribosomal RNA sequence data.–J. Phycol. 26: 711–721, 1990.Google Scholar
  118. Kato H.E., Inoue K., Kandori H. et al.: The light-driven sodium ion pump: a new player in rhodopsin research.–Bioessays 38: 1274–1282, 2016.PubMedGoogle Scholar
  119. Key T., McCarthy A., Campbell D.A. et al.: Cell size trade-offs govern light exploitation strategies in marine phytoplankton.–Environ. Microbiol. 12: 95–104, 2009.PubMedGoogle Scholar
  120. Kiang N.Y., Segura A., Tinetti G. et al.: Spectral signatures of photosynthesis. II. Coevolution with other stars and the atmosphere on extrasolar worlds.–Astrobiology 7: 252–274, 2007b.PubMedGoogle Scholar
  121. Kiang N.Y., Siefert J., Govindjee et al.: Spectral signatures of photosynthesis. I. Review of Earth organisms.–Astrobiology 7: 222–251, 2007aPubMedGoogle Scholar
  122. Kirchman D.L., Hanson T.E.: Bioenergetics of photoheterotrophic bacteria in the oceans.–Env. Microbiol. Rep. 5: 188–199, 2013.Google Scholar
  123. Kirk J.T.O. A theoretical analysis of the contribution of algal cells to the attenuation of light within natural waters. I. General treatment of suspensions of pigmented pigmented cells.–New Phytol. 75: 11–20. 1975a.Google Scholar
  124. Kirk J.T.O. A theoretical analysis of the contribution of algal cells to the attenuation of light within natural waters. II. Spherical cells.–New Phytol. 75: 21–36. 1975b.Google Scholar
  125. Kirk J.T.O. A theoretical analysis of the contribution of algal cells to the attenuation of light within natural waters. III. Cylindrical and spheroidal cells.–New Phytol. 76: 341-258. 1976.Google Scholar
  126. Kirk J.T.O.:–Light and Photosynthesis in Aquatic Ecosystems. 3rd Edition. Pp. 649. Cambridge University Press, Cambridge UK, 2011.Google Scholar
  127. Klamt S., Grammel H., Straube R. et al.: Modelling the electron transport chain of purple non-sulfur bacteria.–Mol. Syst. Biol. 4: 156, 2008.PubMedPubMedCentralGoogle Scholar
  128. Klughammer C., Schreiber U.: Apparent PS II absorption crosssection and estimation of mean PAR in optically thin and thick suspensions of Chlorella.–Photosynth. Res. 123: 77–92, 2015.PubMedGoogle Scholar
  129. Koehne B., Elli G., Jennings R.C. et al.: Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp.–BBA-Bioenergetics 1412: 94–107, 1999.PubMedGoogle Scholar
  130. Koh E.Y., Atamna-Ismaeel N., Martin A. et al.: Proteorhodopsinbearing bacteria in Antarctic sea ice.–Appl. Environ. Microb. 76: 5918–5925, 2010.Google Scholar
  131. Kolber Z.S., van Dover C.L., Niederman R.A. et al.: Bacterial photosynthesis in surface waters of the open ocean.–Nature 407: 177–179, 1991.Google Scholar
  132. Kolber Z.S., Plumley F.G., Lang A.S. et al.: Contribution of photoheterotrophic bacteria to the carbon cycle in the ocean.–Science 292: 2492–2495, 2001.PubMedGoogle Scholar
  133. Kolber Z.S., van Dover C.L., Niederman R.A. et al.: Bacterial photosynthesis in surface waters of the open ocean.–Nature 407: 177–179, 2000.PubMedGoogle Scholar
  134. Kotabová E., Jarešová J., Kaňa R. et al.: Novel type of red-shifted chlorophyll a antenna complex from Chromera velia. I. Physiological relevance and functional connection to photosystems.–Biochim. Biophys. Acta 1837: 734–743, 2014.PubMedGoogle Scholar
  135. Krauss S., Fichtinger B., Lammer H. et al.: Solar flares as a proxy for the young Sun: Satellite observed thermosphere response to an X17.2 flare of Earth’s upper atmosphere.–Ann. Geophys. 30: 1129–1141, 2012.Google Scholar
  136. Kübler J.E., Raven J.A.: Nonequilibrium rates of photosynthesis and respiration under dynamic light supply.–J. Phycol. 32: 963–969, 1996.Google Scholar
  137. Kühl M., Fenchel T.: Bio-optical characteristics and the vertical distribution of photosynthetic pigments and photosynthesis in an artificial cyanobacterial mat.–Microb. Ecol. 4: 94–103, 2000.Google Scholar
  138. Kume A., Akitsu T., Nasahara K.N.: Leaf color is fine-tuned on the solar spectra to avoid strand direct solar radiation.–J. Plant Res. 129: 615–624, 2016.PubMedGoogle Scholar
  139. Kume A.: Importance of the green color, absorption gradient, and spectral absorption of chloroplasts for the radiation energy balance of leaves.–J. Plant Res. 130: 501–514, 2017.PubMedGoogle Scholar
  140. La Roche J., van der Staay G.W.M., Partensky F. et al.: Independent evolution of the prochlorophyte and green plant chlorophyll a/b light harvesting proteins.–P. Natl. Acad. Sci. USA 93: 15244–15248, 1996.Google Scholar
  141. Lange O.L., Kidron G.J., Budel B. et al.: Taxonomic composition and photosynthetic characteristics of the `Biological Soil Crusts’ covering sand dunes in the Western Negev Desert.–Funct. Ecol. 6: 519–527, 1992.Google Scholar
  142. Larkum A.W.D.: The Evolution of Chlorophylls.–In: Scheer H. (ed.): Chlorophylls. Pp. 367–383. CRC Publ., Boca Raton 1991.Google Scholar
  143. Larkum A.W.D.: Light-harvesting systems in algae.–In: Larkum A.W.D., Douglas S.E., Raven J.A. (ed.): Photosynthesis of Algae. Pp. 277–304. Kluwer Acad. Publ., Dordrecht 2003.Google Scholar
  144. Larkum A.W.D.: The evolution of chlorophylls and photosynthesis.–In: Grimm B., Porra R.J., Rüdiger E., Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls: Biochemistry, Biophysics, Functions and Applications. Advances in Photosynthesis and Respiration, Vol. 25. Pp. 261–282. Springer, New York 2006.Google Scholar
  145. Larkum A.W.D.: Evolution of the reaction centers and photosystems.–In: Renger G. (ed.): Primary Processes of Photosynthesis: Principles and Apparatus, Vol. 2. Pp. 489–521. Royal Society of Chemistry, Cambridge 2008.Google Scholar
  146. Larkum A.W.D. and Barrett J.: Light Harvesting Processes in Algae. Advances in Botanical Research 10, 1–219. Academic Press, New York, 1983.Google Scholar
  147. Larkum A.W.D., Scaramuzzi C., Cox G.C. et al.: Lightharvesting chlorophyll c-like pigment in Prochloron.–P. Natl. Acad. Sci. USA 91: 678–683, 1994.Google Scholar
  148. Larkum A.W.D, Lockhart P.J., Howe C.J.: Shopping for plastids.–Trends Plant Sci. 12: 189–195, 2007.PubMedGoogle Scholar
  149. Latasa M., Scharek R., Le Gall F. et al.: Pigment suites and taxonomic group in Prasinophyceae.–J. Phycol. 40: 1149–1155, 2004.Google Scholar
  150. Leliaert F., Tronholm A., Lemieux C. et al.: Chloroplast phylogenomic analysis reveal the deepest-branching lineage of the Chlorophyta, Palmophyllophyceae class nov.–Sci. Rep. 6: 25367, 2016.PubMedPubMedCentralGoogle Scholar
  151. Lenton T.M., Daines S.J.: Matworld–the biogeochemical effects of early life on land.–New Phytol. 215: 531–537, 2017.PubMedGoogle Scholar
  152. Li X., Koblížek M., Feng F. et al.: Whole-genome sequence ofa freshwater aerobic anoxygenic phototroph, Porphyrobacter sp. strain AAP82, isolated from the Huguangyan Maar Lake in Southern China.–Genome Announc. 1: e00034–13, 2013.PubMedPubMedCentralGoogle Scholar
  153. Li Y-Q., Scales N., Blankenship R.E. et al.: Extinction coefficient for red-shifted chlorophylls: Chlorophyll d and chlorophyll f.–BBA-Bioenergetics 1817: 1292–1298, 2012PubMedGoogle Scholar
  154. Lichtenberg M., Kühl M.Y.: Pronounced gradients of light, photosynthesis and O2 consumption in the tissue of the brown alga Fucus serratus.–New Phytol. 207: 559–569, 2015.PubMedGoogle Scholar
  155. Litchman E.: Growth rates of phytoplankton under fluctuating light.–Freshwater Biol. 44: 223–235, 2000.Google Scholar
  156. Loughlin P., Lin Y., Chen M.: Chlorophyll d and Acayochloris marina: current status.–Photosynth. Res. 116: 277–293, 2013.PubMedGoogle Scholar
  157. Loughlin P.C., Willows R.D., Chen M.: In vitro conversion of vinyl to formyl groups in naturally occurring chlorophylls.–Sci. Rep. 4: 6069, 2014.PubMedPubMedCentralGoogle Scholar
  158. Lüning K., Dring M.R.: Action spectra and spectral quantum yield of photosynthesis in marine macroalgae with thin and thick thalli.–Mar. Biol. 87: 119–129, 1985.Google Scholar
  159. Lüning K.: Seaweeds. Their Environment, Biogeography, and Ecophysiology. Pp. 527. John Wiley & Sons, New York 1990.Google Scholar
  160. Lyell C.: On fossil rain-marks of the Recent, Triassic and Carboniferous periods.–J. Geol. Soc. 7: 338–347, 1851.Google Scholar
  161. Man D., Wang W., Sabehei G. et al.:. Diversification and spectral tuning in marine proteorhodopsin.–EMBO J. 22: 1725–1731, 2003.PubMedPubMedCentralGoogle Scholar
  162. Mareš J., Hrouzek P., Kaňa R. et al.: The primitive thylakoid-less cyanobacterium Gloeobacter is a common rock-dwelling organism.–PLoS ONE 8: e66323, 2013.PubMedPubMedCentralGoogle Scholar
  163. Marchetti A., Schruth D.M., Durkin C.A. et al.: Comparative metatranscriptomics identifies molecular basis for the physiological response phytoplankton to varying iron availability.–P. Natl. Acad. Sci. USA 109: E317–E325, 2012.Google Scholar
  164. Markager S.: Light absorption and quantum yield for growth in five species of marine macroalga.–J. Phycol. 29: 54–63, 1993.Google Scholar
  165. Markager S., Sand-Jensen K.: Light requirement and depth zonation of marine macroalgae.–Mar. Biol. Prog. Ser. 88: 83–92, 1992Google Scholar
  166. Marosvölgyi M.A., van Gorkum H.J.: Cost and color of photosynthesis.–Photosynth. Res. 103: 105–109, 2010.PubMedPubMedCentralGoogle Scholar
  167. Mathusamy S., Baltar F., González J.M. et al.: Dynamics of metabolic activities and gene expression in the roseobacter clade bacterium Phaeobacter sp. strain med153 during growth with thiosulfate.–Appl. Environ. Microbiol. 80: 6933–6942, 2014.Google Scholar
  168. Matsunoto-Yagi A., Mukohata Y.: Two possible roles of bacteriorhodopsin; a comparative study of strains of Halobacterium halobium differing in pigmentation.–Biochem. Bioph. Res. Co. 78: 237–243, 1977.Google Scholar
  169. Mauzerall D.: Why chlorophyll?–Ann. NY Acad. Sci. 206: 483–494, 1973.PubMedGoogle Scholar
  170. Meeks J.C.: Chlorophylls.–In: Stewart W.D.P. (ed.): Algal Physiology and Biochemistry. Pp. 161–175. Blackwell, Oxford 1974.Google Scholar
  171. Merbs S.L., Nathans J.: Absorption spectra of human cone pigments.–Nature 356: 433–435, 1992.PubMedGoogle Scholar
  172. Michel H., Oesterhelt D.: Electrochemical proton gradient across the cell membrane of Halobacterium halobium: effect of N,N’-dicyclohexylcarbodiimide, relation to adenosine triphosphate, adenosine diphosphate and phosphate concentration, and influence of the potassium gradient.–Biochemistry 19: 4607–4614, 1980.PubMedGoogle Scholar
  173. Milo R.: What governs the reaction centre excitation wavelengths of photosystems I and II.–Photosynth. Res. 101: 59–67, 2009.PubMedGoogle Scholar
  174. Mimuro M., Hirayani K., Uezono K. et al.: Uphill energy transfer in a chlorophyll d-dominated oxygenic photosynthetic prokaryote, Acaryochloris marina.–Biochim. Biophys. Acta 456: 27–34, 2007.Google Scholar
  175. Miyashita H., Adachi K., Kurazo N. et al.: Pigment composition of a novel oxygenic photosynthetic prokaryote containing chlorophyll d as a major chlorophyll.–Plant Cell Physiol. 38: 274–281, 1997.Google Scholar
  176. Miyashita H., Ikemoto H., Kurano N. et al.: Acaryochloris marina Gen. et Sp. Nov. (Cyanobacteria), an oxygenic photosynthetic prokaryote containing Chl d as a major pigment.–J. Phycol. 39: 1247–1253, 2003.Google Scholar
  177. Miyashita H., Ikemoto H., Kurano N. et al.: Chlorophyll d as a major pigment.–Nature 383: 402–403, 1996.Google Scholar
  178. Mohr R., Voβ B., Schliep M. et al.: A new chlorophyll dcontaining cyanobacterium: evidence for niche adaptation in the genus Acaryochloris.–ISME J. 4: 1456–1469, 2010.PubMedGoogle Scholar
  179. Morel A., Bricaud A.: Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton.–Deep Sea Res. 28: 1375–1393, 1981.Google Scholar
  180. Morel A., Bricaud A.: Inherent optical properties of algal cells including phytoplankton: theoretical and experimental results.–Can. Bull. Fish. Aquat. Sci. 214: 521–559, 1986.Google Scholar
  181. Mulkidjanian A.Y., Koonin E.V., Makarova K.S. et al.: The cyanobacterial genome core and the origin of photosynthesis.–P. Natl. Acad. Sci. USA 103: 13126–13131, 2006.Google Scholar
  182. Muyzer G., Stams A.J.M.: The ecology and biotechnology of sulphate-reducing bacteria.–Nat. Rev. Microbiol. 6: 441–454, 2008.PubMedGoogle Scholar
  183. Niedzwiedzki D.M., Liu H., Chen M. et al.: Excited state properties of chlorophyll f in organic solvents at ambient and cryogenic temperatures.–Photosynth. Res. 121: 25–34, 2014.PubMedGoogle Scholar
  184. Nieuwenburg P., Clark R.J. Chen M. et al.: Explanation of proposed “uphill energy transfer” in chlorophyll d, the major pigment of Acaryochloris marina.–Photochem. Photobiol. 77: 628–637, 2003.PubMedGoogle Scholar
  185. Nicholls D.G., Ferguson S.J.: Bioenergetics 4. Pp. 419. Academic Press, Amsterdam 2013.Google Scholar
  186. Nishio J.N.: Why are higher plants green? Evolution of the higher plant photosynthetic pigment complement.–Plant Cell Environ. 23: 539–548, 2000.Google Scholar
  187. Nutman A.P., Bennett V.C., Friend C.R.L. et al.: Rapid emergence of life shown by discovery of 3,700-million-yearold microbial structures.–Nature 537: 535–538, 2016.PubMedGoogle Scholar
  188. Oesterhelt D., Hegemann P., Tittor J.: The photocycle of the chloride pump halorhodopsin. II: Quantum yields and a kinetic model.–EMBO J. 4: 2351–2356, 1985.PubMedPubMedCentralGoogle Scholar
  189. Oesterhelt D., Stoeckenius W.: Rhodopsin-like protein from the purple membrane of Halobacterium halobium.–Nature New Biol. 233: 149–152, 1970.Google Scholar
  190. Ohashi S., Miyashita H., Okada N. et al.: Unique photosystems in Acaryochloris marina.–Photosynth. Res. 98: 141–149, 2008.PubMedGoogle Scholar
  191. Ohkubo S., Miyashita H.: A niche for cyanobacteria producing chlorophyll f within a microbial mat.–ISME J. 11: 2368–2378, 2017.PubMedGoogle Scholar
  192. Öquist G.: Adaptations in pigment composition and photosynthesis by far red radiation in Chlorella pyrenoidosa.–Physiol. Plantarum 22: 516–528, 1969.Google Scholar
  193. Ort D.R., Merchant S.S., Alric J. et al.: Redesigning photosynthesis to sustainability meet global food and bioenergy demand.–P. Natl. Acad. Sci. USA 112: 8529–8536, 2015.Google Scholar
  194. Palovaara J., Akram N., Baltar F. et al.: Stimulation of growth of proteorhodopsin phototrophy involves regulation of central metabolic pathways in marine planktonic bacteria.–P. Natl. Acad. Sci. USA 111: E3650–E3658, 2014.Google Scholar
  195. Pan H., Slapeta J., Carter D. et al.: Phylogenetic analysis of the light-harvesting system in Chromera velia.–Photosynth. Res. 111: 19–28, 2012.PubMedGoogle Scholar
  196. Pazderník M.: Light harvesting complexes and chromatic adaptation of Eustigmatophyte alga Trachydiscus minutus. MSc Thesis, University of Southern Bohemia, České Budějovice 2015.Google Scholar
  197. Pettai H., Oja V., Freiberg A. et al.: Photosynthetic activity of far-red light in green plants.–BBA-Bioenergetics 1708: 311–321, 2005b.PubMedGoogle Scholar
  198. Pettai H., Oja V., Freiberg A. et al.: The long-wavelength limit of plant photosynthesis.–FEBS Lett. 579: 4017–4019, 2005a.PubMedGoogle Scholar
  199. Pinhassi J., deLong E.F., Béjà, O. et al.: Marine bacterial and archael ion-pumping rhodopsins: genetic diversity, physiology, and ecology.–Microbiol. Mol. Biol. R. 80: 929–954, 2016.Google Scholar
  200. Pirie N.W.: The size of small organisms.–P. Roy. Soc. B-Biol. Sci. 160: 149–166, 1964.Google Scholar
  201. Pirie N.W.: On being the right size.–Annu. Rev. Microbiol. 27: 119–166, 1973.PubMedGoogle Scholar
  202. Poorter L., Oberbauer S.T., Clark D.B.: Leaf optical properties along a vertical gradient in a tropical rain forest canopy in Costa Rica.–Am. J. Bot. 82: 1257–1263, 1995.Google Scholar
  203. Poorter L., Kwant R., Hernández R., Medina E., Werger M.J.A.: Leaf optical properties in Venezuelan cloud forest trees.–Tree Physiol. 20: 519–526, 2000.PubMedGoogle Scholar
  204. Price D.C., Chan C-X., Yoon H-S. et al.: Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants.–Science 335: 843–847, 2012.PubMedGoogle Scholar
  205. Přibyl P., Eliáš M., Cepák V. et al.: Zoosporogenesis, morphology, ultrastructure, pigment composition and phylogenetic position of Trachydiscus minutus (Eustigmatophyceae, Heterokontophyta).–J. Phycol. 48: 231–242, 2012.PubMedGoogle Scholar
  206. Rafique R., Zhao F., de Jong R. et al.: Global and regional variability and change in terrestrial ecosystems in net primary productivity and NDVI: a model-data comparison.–Remote Sens.-Basel 8: 177, 2016.Google Scholar
  207. Raven J.A.: A cost-benefit analysis of photon absorption by photosynthetic unicells.–New Phytol. 98: 583–625, 1984.Google Scholar
  208. Raven, J.A. Evolution of plant life forms.–In: Givnish T (ed.): On the Economy of Plant Form and Function. Pp. 421–492. Cambridge University Press, Cambridge 1986a.Google Scholar
  209. Raven J.A. Physiological consequences of extremely small size for autotrophic organisms in the sea.–In: Platt T, Li W.K.W. (ed.): Photosynthetic Picoplankton. Pp. 1–70. Department of Fisheries and Oceans, Ottawa 1986b.Google Scholar
  210. Raven J.A.: The bigger the fewer: size, taxonomic diversity and the range of chlorophyll(ide) pigments in oxygen evolving marine photolithotrophs.–J. Mar. Biol. Assoc. UK 76: 211–217, 1996Google Scholar
  211. Raven J.A.: Small is beautiful. The picophytoplankton.–Funct. Ecol. 12: 503–513. 1998.Google Scholar
  212. Raven J.A.: Picophytoplankton.–Prog. Phycol. Res. 13: 33–106, 1999.Google Scholar
  213. Raven J.A.: Astrobiology. Photosynthesis in watercolours.–Nature 448: 418, 2007.PubMedGoogle Scholar
  214. Raven J.A.: Functional evolution of photochemical energy transformation in oxygen-producing organisms.–Funct. Plant Biol. 36: 505–515, 2009a.Google Scholar
  215. Raven J.A.: Contribution of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments.–Aquat. Microb. Ecol. 56: 177–192, 2009b.Google Scholar
  216. Raven J.A.: Evolution and palaeophysiology of the vascular system and other means of long distance transport.–Philos. T. R. Soc. B 373: 20160497, 2018.Google Scholar
  217. Raven J.A., Smith F.A.: H+ transport in the evolution of photosynthesis.–Biosystems 14: 95–111, 1981.PubMedGoogle Scholar
  218. Raven J.A., Cockell C.S.: Influence on photosynthesis of starlight, moonlight, planetlight and light pollution (Reflections on photosynthetically active radiation in the universe).–Astrobiology 6: 668–675, 2006.PubMedGoogle Scholar
  219. Raven J.A., Hurd C.J.: Ecophysiology of photosynthesis in macroalgae.–Photosynth. Res. 113: 105–125, 2012.PubMedGoogle Scholar
  220. Raven J.A., Ralph P.J.: Enhanced biofuel production using optimality, pathway modification and waste minimization.–J. Appl. Phycol. 27: 1–31, 2015.Google Scholar
  221. Raven J.A., Beardall J.: The ins and outs of CO2.–J. Exp. Bot. 67: 1–13, 2016.PubMedGoogle Scholar
  222. Raven J.A., Kübler J.E., Beardall J.: Put out the light, then put out the light.–J. Mar. Biol. Assoc. UK 80: 1–25, 2000.Google Scholar
  223. Raven J.A., Wolstencroft R.D.: Constraints on photosynthesis on Earth and Earth-like planets.–In: Norris, R.P., Stooman, F.H. (ed.): Bioastronomy: Life among the Stars. Proceedings of the 213th Symposium of the International Astronomical Union. Hamilton Island, Great Barrier Reef, Australia. Pp. 305–308. Astronomical Society of the Pacific, San Francisco, USA, 2002.Google Scholar
  224. Raven J.A., Beardall J., Flynn K.J., Maberly S.C.: Phagotrophy in the origins of photosynthesis in eukaryotes and as a complementary mode of nutrition in phototrophs: relation to Darwin’s Insectivorous Plants.–J. Exp. Bot. 60: 3975–3987, 2009.PubMedGoogle Scholar
  225. Raven J.A., Beardall J., Larkum A.W.D., Sanchez-Baracaldo P.: Interaction of photosynthesis with genome size and function.–Philos. T. Roy. Soc. B 368: 20120264, 2013a.Google Scholar
  226. Raven J.A., Donnelly S.: Brown Dwarfs and Black Smokers: the potential for photosynthesis using radiation from lowtemperature black bodies.–In: de Vera J.-P., Seckbach J. (ed.): Habitats of other Planets and Satellites, Cellular Origin, Life in Extreme Habitats and Astrobiology. Pp. 267–284. Springer, Dordrecht 2013b.Google Scholar
  227. Raven J.A., Beardall, J., Giordano M.: Energy cost of carbon dioxide concentrating mechanisms in aquatic organisms.–Photosynth. Res. 121: 111–124, 2014.PubMedGoogle Scholar
  228. Raven J.A., Beardall J., Sánchez-Baracaldo P.: The possible evolution and future of CO2 concentrating mechanisms.–J. Exp. Bot. 68: 3701–3716, 2017.PubMedGoogle Scholar
  229. Reimers J.R., Cai Z.-L., Kobayashi R. et al.: Assignment of the Q-bands of the chlorophylls: coherence loss via Qx - Qy Mixing.–Sci. Rep-UK 3: 2761, 2013.Google Scholar
  230. Rexroth S., Mullineaux C.W., Ellinger E. et al.: The plasma membrane of the cyanobacterium Gloeobacter violaceous contains segregated bioenergetics domains.–Plant Cell 23: 2379–2390, 2011.PubMedPubMedCentralGoogle Scholar
  231. Ritchie R.J.: Fitting light saturation curves measured using PAM fluorometry.–Photosynth. Res. 96: 201–215, 2008.PubMedGoogle Scholar
  232. Ritchie R.J.: The use of solar radiation by a photosynthetic bacterium, Rhodopseudomonas palustris: Model simulation of conditions found in a shallow pond or flatbed reactor.–Photochem. Photobiol. 89: 1143–1162, 2013PubMedGoogle Scholar
  233. Ritchie R.J.: Photosynthesis in an encrusting Lĺichen (Dirinaria picta (Sw.) Schaer.ex Clem., Physiaceae) and its symbiont, Trebouxia sp, using PAM fluorometry.–Int. J. Plant Sci. 175: 450–466, 2014.Google Scholar
  234. Ritchie R.J., Runcie J.W.: Photosynthetic electron transport in an oxygenic photosynthetic bacterium Afifella (Rhodopseudomonas) marina measured using PAM fluorometry.–Photochem. Photobiol. 89: 370–383, 2013.PubMedGoogle Scholar
  235. Ritchie R.J., Runcie J.W.: A portable reflectance-absorptancetransmittance meter for photosynthetic work on vascular plant leaves.–Photosynthetica 52: 614–626, 2014.Google Scholar
  236. Ritchie R.J., Mekjinda N.: Measurement of photosynthesis using PAM technology in a purple sulphur bacterium Thermochromatium tepidum (Chromatiaceae).–Photochem. Photobiol. 91: 350–358, 2015.PubMedGoogle Scholar
  237. Ritchie R.J., Larkum A.W.D., Ribas I.: Could photosynthesis function on Proxima Centauri b?–Int. J. Astrobiol. 2017: 1–30, 2017Google Scholar
  238. Rosing M.T., Frei R.: U-rich Archaean sea-floor sediments from Greenland–indications of > 3700 Ma oxygenic photosynthesis.–Earth Planet. Sc. Lett. 217: 237–244, 2004.Google Scholar
  239. Rowan K.S.: Photosynthetic Pigments of Algae. Pp. 334. Cambridge University Press, Cambridge 1989.Google Scholar
  240. Runcie J.W., Gurgel,C.F., Mcdermid K.J.: In situ photosynthetic rates of tropical marine macroalgae at their lower depth limit.–Eur. J. Phycol. 43: 377–388, 2008.Google Scholar
  241. Sabehi G., Kirkup B.C., Rozenberg M.: Adaptation and spectral tuning in divergent marine proteorhodopsins from the eastern Mediterranean and the Sargasso Sea.–ISME J. 1: 49–55, 2007.Google Scholar
  242. Sánchez-Baracaldo P., Pisani D., Raven J.A. et al.: Early photosynthetic eukaryotes inhabited low-salinity habitats.–P. Natl. Acad. Sci. USA 114: E7727–E7746, 2017.Google Scholar
  243. Sánchez-Baracaldo P., Ridgwell P., Raven J.A.: A neoproterozoic transition in the marine nitrogen cycle.–Curr. Biol. 24: 652–657, 2014.PubMedGoogle Scholar
  244. Sánchez-Baracaldo P.: Origin of marine planktonic cyanobacteria.–Sci. Rep.-UK 5: 17418, 2015.Google Scholar
  245. Saw J.H.W., Schatz M., Brown M.V. et al.: Cultivation and complete genome sequencing of Gloeobacter kilaueensis sp. nov., from a lava cave in Kīlauea Caldera, Hawai’i.–PLoS ONE 8: e76376, 2013.PubMedPubMedCentralGoogle Scholar
  246. Seatae P., Bunthawi, S., Ritchie R.J.: Environmental persistence of chlorine from prawn farm discharge monitored by measuring the light reactions of photosynthesis of phytoplankton.–Aquacult. Int. 22: 321–338, 2014.Google Scholar
  247. Selosse M.-A., Charpin M., Not F.: Mixotrophy everywhere on land and in the water: the grand écourt hypothesis.–Ecol. Lett. 20: 246–263, 2017.PubMedGoogle Scholar
  248. Senge M.O., Smith K.M.: Biosynthesis and Structures of the Bacteriochlorophylls.–In: Blankenship R.E., Madigan M.T., Bauer C.E. (ed): Anoxygenic Photosynthetic Bacteria. Pp. 137–151. Kluwer Academic Publishers, Dordrecht 1995.Google Scholar
  249. Shih P. M., Hemp J., Ward L.M. et al.: Crown group Oxyphotobacteria postdate the rise of oxygen.–Geobiology 15: 19–29, 2017.PubMedGoogle Scholar
  250. Scheer H.: An overview of chlorophylls and bacteriochlorophylls: biochemistry, biophysics, functions and applications–In: Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls. Pp. 1–26. Springer, Dordrecht 2006.Google Scholar
  251. Scheer H.: Structure and occurrence of chlorophylls.–In: Scheer H. (ed.): Chlorophylls and Bacteriochlorophylls. Pp. 3–30. CRC Press, Boca Raton 1991.Google Scholar
  252. Schirrmeister B.E., Sánchez-Baracaldo P., Wacey D.: Cyanobacterial evolution during the Precambrian.–Int. J. Astrobiol. 15: 187–204, 2016.Google Scholar
  253. Schliep M., Cavigliasso G., Quinnell R.G. et al.: Formyl group modification of chlorophyll a: a major evolutionary mechanism in oxygenic photosynthesis.–Plant Cell Environ. 36: 521–527, 2013.PubMedGoogle Scholar
  254. Schliep M., Crossett B., Willows R.D. et al.: O-18 labeling of chlorophyll d in Acaryochloris marina reveals that chlorophyll a and molecular oxygen are precursors.–J. Biol. Chem. 285: 28450–28456, 2010.PubMedPubMedCentralGoogle Scholar
  255. Schliep M., Chen M., Larkum T. et al.: The function of MgDVP in a chlorophyll d-containing organism.–Photosynth. Res. 91: 263–263, 2007.Google Scholar
  256. Schlodder E., Lendzian F., Meyer J. et al.: Long-wavelength limit of photochemical energy conversion in photosystem I.–J. Am. Chem. Soc. 136: 3904–3918, 2014.PubMedPubMedCentralGoogle Scholar
  257. Schmidt S., Raven J.A., Paungfoo-Lonhienne C.: The mixotrophic nature of photosynthetic plants.–Funct. Plant Biol. 40: 425–438, 2013.Google Scholar
  258. Schobert B., Lanyi J.K.: Halorhodopsin is a light-driven chloride pump.–J. Biol. Chem. 257: 10306–10313, 1982.PubMedGoogle Scholar
  259. Skelton A.E., Catchpole G., Abbott J.T. et al.: Biological origins of color categorization.–P. Natl. Acad. Sci. USA 114: 5545–5550, 2017.Google Scholar
  260. Slamowitz C.H., Okamoto N., Burri L. et al.: A bacterial proteorhodopsin proton pump in marine eukaryotes.–Nat. Commun. 2: 183, 2011.Google Scholar
  261. SMARTS: Simple Model of Atmospheric Radiative Transfer of Sunshine (SMARTS): {unhttp://www.nrel.gov/rredc/smarts/ [Accessed 12/Aug/2011].Google Scholar
  262. Som S.M., Buick R., Hagadorn J.W. et al.: Earth’s air pressure 2.7 billion years ago constrained to less than half of present levels.–Nat. Geosci. 9: 448–451, 2016.Google Scholar
  263. Som S.M., Catling D.C., Hornmeijer J.P. et al.: Air density billion years ago limited to less than twice modern levels.–Nature 484: 359–362, 2012.PubMedGoogle Scholar
  264. Soo R.M., Hemp J., Parks D.H. et al.: On the origins of oxygenic photosynthesis and aerobic respiration in cyanobacteria.–Science 355: 1436–1440, 2017.PubMedGoogle Scholar
  265. Soo R.M., Skennerton C.T., Sekiguchi Y. et al.: An expanded genomic representation of the phylum cyanobacteria.–Genome Biol. Evol. 6: 1031–1045, 2014.PubMedPubMedCentralGoogle Scholar
  266. Sparks W.B., DasSarma S., Reid I.N.: Evolutionary competition between primitive systems: existence of an early purple Earth?–In: Bulletin of the American Astronomical Society, Vol. 38. Pp. 901. University of Maryland Biotechnology Institute, Maryland 2007.Google Scholar
  267. Stoecker D.K., Hansen P.J., Caron D.A. et al.: Mixotrophy in the marine plankton.–Annu. Rev. Mar. Sci. 9: 311–335, 2017.Google Scholar
  268. Stomp M., Huisman J., Stal L.J. et al.: Colorfull niches of phototrophic microorganisms shaped by vibrations of the water molecules.–ISME J. 1: 271–282, 2007.PubMedGoogle Scholar
  269. Suomivuori C-M., Gamiz-Hernandez A.P., Sundholm D. et al.: Energetics and dynamics of a light-driven sodium-pumping rhodopsin.–P. Natl. Acad. Sci. USA 114: 7043–7048, 2017.Google Scholar
  270. Telfer A., Pascal A., Barber J. et al.: Electron transfer reactions in photosystem I and II of the chlorophyll d containing cyanobacterium, Acaryochloris marina.–Photosynth. Res. 91: 143–143, 20Google Scholar
  271. Thapper A., Madedor F., Mokvist F. et al.: Defining the far-red limit of photosystem II in spinach.–Plant Cell 21: 2381–2401, 2009.Google Scholar
  272. Tice M.M., Lowe D.R.: Photosynthetic microbial mats in the 3,416-Myr-old ocean.–Nature 431: 549–552, 2004.PubMedGoogle Scholar
  273. Tomitani A., Okada K., Miyashita H. et al.: Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts.–Nature 400: 159–162, 1999.PubMedGoogle Scholar
  274. Tomkins A.G., Bowlt L., Genge M. et al.: Ancient micrometeorites suggestive of oxygen-rich Archaean upper atmosphere.–Nature 533: 235–238, 2016.PubMedGoogle Scholar
  275. Toms T., Shinoda T., Chen M. et al.: Energy transfer processes in chlorophyll f-containing cyanobacteria using time-resolved fluorescence spectroscopy on intact cells.–Biochim. Biophys. Acta 1837: 1484–1489, 2014.Google Scholar
  276. Trissl H.W.: Modelling the excitiation energy capture in thylakoid membranes.–In: Larkum A.W.D., Douglas S.E. Raven J.A. (ed.): Photosynthesis in Algae. Pp. 245–276. Springer Verlag, Berlin 2003.Google Scholar
  277. Tsukamoto T., Yoshizawa S., Kikukawa T. et al.: Implications for light driven chloride ion transport mechanism of Nonlabens marinus Rhodopsin 3 by its photochemical characteristics.–J. Phys. Chem. B 121: 2027–2038, 2017.PubMedGoogle Scholar
  278. Tsunuda S.P., Ewers D.O., Gazzarrini S. et al.: H+-pumping rhodopsin from the marine alga Acetabularia.–Biophys. J. 91: 1471–1479, 2006.Google Scholar
  279. Vásquez-Elizondo R.M., Legaria-Moreno L., Pérez-Castro M.A. et al.: Absorptance determinations on multicellular tissues.–Photosynth. Res. 132: 311–324, 2017.PubMedGoogle Scholar
  280. Vogl K., Tank M., Orf G.S. et al.: Bacteriochlorophyll f: properties of chlorosomes containing the “forbidden chlorophyll”.–Front. Microbiol. 3: 298, 2012.PubMedPubMedCentralGoogle Scholar
  281. Vopel K., Hawes I.: Photosynthetic performance of benthic microbial mats in Lake Hoare, Antarctica.–Limnol. Oceanogr. 51: 1801–1812, 2006.Google Scholar
  282. Wakao N., Yokoi N., Isoyama N. et al.: Discovery of natural photosynthesis using Zn-containing bacteriochlorophyll in an aerobic bacterium Acidophilium rubrum.–Plant Cell Physiol. 37: 889–893, 1996.Google Scholar
  283. Waters E.R.: Molecular adaptation and the origin of land plants.–Mol. Phylogenet. Evol. 29: 456–463, 2003.PubMedGoogle Scholar
  284. Wellman C.H., Strother P.K.: The terrestrial biota prior to the origin of land plants (embryophytes): a review of the evidence.–Palaeontology 58: 601–627, 2015.Google Scholar
  285. Wilhelm C., Jakob T.: Uphill energy transfer from longwavelength absorbing chlorophylls to PSII in Ostreobium sp. is functional in carbon assimilation.–Photosynth. Res. 87: 323–329, 2006.PubMedGoogle Scholar
  286. Williams P.J.leB., Laurens L.M.L.: Microalgae as biodiesel and biomass feedstocks: review and analysis of the biochemistry, energetics and economics.–Energ. Environ. Sci. 3: 554–590, 2010.Google Scholar
  287. Willows R.D., Li Y., Scheer H. et al.: Structure of chlorophyll f.–Org. Lett. 15: 1588–1590, 2013.PubMedGoogle Scholar
  288. Wolf B.J., Niedzwiedzki D.M., Magdaong N.C.M. et al.: Characterizarion of a newly isolated Eustigmatophyte alga capable of ultilizing far-red light as its sole light source.–Photosynth. Res. doi: 10.1007.s11120-017-0401-z, in press, 2017.Google Scholar
  289. Wolstencroft R.D., Raven J.A.: Photosynthesis: likelihood of occurrence and possibility of detection on Earth-like planets.–Icarus 157: 535–548, 2002.Google Scholar
  290. Wraight C.A., Clayton R.K.: The absolute quantum efficiency of bacteriochlorophyll photo-oxidation in reaction centres of Rhodopseudomonas spheroides.–Biochim. Biophys. Acta 333: 246–260, 1974.PubMedGoogle Scholar
  291. Yoshizawa S., Kumagai Y., Kim H. et al.: Functional characterisation of flavobacteria rhodopsins reveal a unique class of light-driven chloride pump in bacteria.–P. Natl. Acad. Sci. USA 111: 6732–6737, 2014.Google Scholar
  292. Yurkov V., Beatty J.T.: Aerobic anoxygenic photosynthetic bacteria.–Microbiol. Mol. Biol. Rev. 62: 695–724, 1998.PubMedPubMedCentralGoogle Scholar
  293. Yutin N., Koonin E.V.: Proteorhodopsin genes in giant viruses.–Biol. Direct 7: 34, 2012.PubMedPubMedCentralGoogle Scholar
  294. Zak E., Norling B., Maitra R. et al.: The initial steps of biogenesis of cyanobacterial photosystems occur in plasma membranes.–P. Natl. Acad. Sci. USA 98: 13443–13448, 2001.Google Scholar
  295. Zapata M., Garrido J.L.: Occurrence of phytylated chlorophyll c in Isochrysis galbana and Isochrysis sp. (Clone T-Iso) (Prymnesiophyceae).–J. Phycol. 33: 209–214, 1997.Google Scholar
  296. Zeng Y., Feng F., Liu Y. et al.: Genome sequences and photosynthetic gene cluster composition of a freshwater aerobic anoxygenic phototroph, Sandarakinorhabdus sp. strain AAP62, isolated from the Shahu Lake of Ningxia, China.–Genome Announc. 1: e00034–13, 2013a.PubMedPubMedCentralGoogle Scholar
  297. Zeng Y., Koblížek M., Feng F. et al.: Whole-genome sequence of an aerobic anoxygenic phototroph, Blastomonas sp. strain AAP 53, isolated from a freshwater desert lake in inner Mongolia, China.–Genome Announcements 1: e00071–13, 2013b.PubMedCentralGoogle Scholar
  298. Zheng Q., Liu Y., Sun J. et al.: Whole-genome sequence of aerobic anoxygenic phototrophic bacterium Erythrobacter sp. JL457, isolated from the South China Sea.–Mar. Genom. 21: 15–16, 2015.Google Scholar
  299. Zhu X.G., Long S.P., Ort D.R.: What is the maximum efficiency with which photosynthesis can convert solar energy into biomass.–Curr. Opin. Biotech. 19: 153–159, 2008.PubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  • A. W. D. Larkum
    • 1
  • R. J. Ritchie
    • 2
  • J. A. Raven
    • 3
    • 1
  1. 1.Global Climate Cluster, Building 4University of Technology SydneyBroadwayAustralia
  2. 2.Tropical Environmental Plant Biology Unit, Faculty of Technology and EnvironmentPrince of Songkla University PhuketKathu, PhuketThailand
  3. 3.University of Dundee at the James Hutton InstituteInvergowrie, DundeeUK

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