Functional evolution of photochemical energy transformations in oxygen-producing organisms

Functional Plant Biology

Volumn 36, Issue 6, 2009, Pages 505-515

  Raven, John A ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Chlorophyll a; Photosynthesis; Retinal

Indexed keywords

CARBON DIOXIDE REDUCTION; CHLOROPHYLL A; ENERGETIC PROPERTIES; ENERGY TRANSFORMATION; HIGH RATE; IN-VIVO; ION PUMPING; LONG-WAVELENGTH LIMITS; OXYGEN PRODUCTION; OXYGENIC PHOTOSYNTHESIS; OXYGENIC PHOTOTROPHS; RETINAL;

ALDEHYDES; CARBON DIOXIDE; CHROMOPHORES; OPHTHALMOLOGY; OXYGEN; PHOTOSYNTHESIS; PORPHYRINS; SOLAR ENERGY;

CHLOROPHYLL;

BIOENERGETICS; CARBON DIOXIDE; CHLOROPHYLL A; PHOTOCHEMISTRY; PHOTOSYNTHESIS; PHYSIOLOGY;

EID: 67650085797     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP09087     Document Type: Review

References (88)

1. Alberte RS (1989) Physiological and cellular features of Prochloron. In 'Prochloron: a microbial enigma'. (Eds RA Lewin, L Chang) pp. 31-52. (Chapman and Hall: New York)
2. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends in Plant Science 8, 15-19. doi: 10.1016/ S1360-1385(02)00006-7
3. 6 f: structure for signalling and vectorial metabolism. Trends in Plant Science 9, 130-137. doi: 10.1016/j.tplants.2004.01.009
4. Allen JF (2005) A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Letters 579, 963-968. doi: 10.1016/j.febslet.2005.01.015
5. Allen JF, Martin W (2007) Out of thin air. Nature 445, 610-612. doi: 10.1038/445610a
6. Atamna-Ismaeel N, Sabehi G, Sharon I, Wizel K-P, Labrenz M, Jürgens K, Barkay T, Stomp M, Huisman J, Beja O (2008) Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems. The ISME Journal 2, 656-662. doi: 10.1038/ismej.2008.27
7. Beard SJ, Davis PA, Iglesias-Rodríguez D,Skulberg OM, Walsby AE (2000) Gas vesicle genes in Planktothrix spp. from Nordic lakes: strains with weak gas vesicles possess a larger variant of gupC. Microbiology (Reading, England) 146, 2009-2018.
8. Belkin S, Mehlhorn RJ, Packer L (1987) Proton gradients in intact cyanobacteria. Plant Physiology 84, 25-30. doi: 10.1104/pp.84.1.25
9. Beust H, Bonfils X, Delfosse X, Udry S (2008) Dynamical evolution of the Gliese 581 planetary system. Astronomy & Astrophysics 479, 277-282. doi: 10.1051/0004-6361:20078794
10. Björn LO, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynthesis Research 99, 85-98. doi: 10.1007/s11120-008-9395-x
11. Bryant DA, Friggard N-U (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends in Microbiology 14, 488-496. doi: 10.1016/j.tim.2006.09.001
12. Clausen J, Junge W (2008a) The terminal reaction cascade of water oxidation: proton and oxygen release. Biochimica et Biophysica Acta 1777, 1311-1318. doi: 10.1016/j.bbabio.2008.06.009
13. Clausen J, Junge W (2008b) The inhibitory effects of acidification and augmentated oxygen pressure on water oxidation. Photosynthesis Research 98, 229-233. doi: 10.1007/s11120-008-9321-2
14. 2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry 44, 12775-12779. doi: 10.1021/bi051183a
15. Cser K, Deák Z, Telfer A, Barbe J, Vass I (2008) Energetics of photosystem II charge recombination in Acaryochloris marina studied by thermoluminescence and flash-induced chlorophyll fluorescence measurements. Photosynthesis Research 98, 131-140. doi: 10.1007/s11120-008-9373- 3
16. Dring MJ (1981) Chromatic adaptation of photosynthesis in benthic algae: an examination of its ecological significance using a theoretical model. Limnology and Oceanography 26, 271-284.
17. Duyens LNM (1956) The flattening of the absorption of suspensions, as compared to that of solutions. Biochimica et Biophysica Acta 19, 1-12. doi: 10.1016/0006-3002(56)90380-8
18. Engelmann TW (1883) Farbeund assimilation. Botanische Zeitung 41,1-29.
19. Falkowski PG, Raven JA (2007) 'Aquatic photosynthesis, 2nd edn'. (Princeton University Press: Princeton)
20. Friedrich T, Geibel S, Kalmbach R, Chizhov I, Ataka K, Heberle J, Engelhard M, Bamberg E (2002) Proteorhodopsin is a light-driven proton pump with variable vectoriality. Journal of Molecular Biology 321, 821-838. doi: 10.1016/S0022-2836(02)00696-4
21. Gloag RS, Ritchie RJ, Chen M, Larkum AWD, Quinnell RG (2007) Chromatic photoacclimation, photosynthetic electron transport and oxygen evolution in the chlorophyll d-containing oxyphotobacterium Acaryochloris marina. Biochimica et Biophysica Acta (BBA) -Bioenergetics 1767, 127-135. doi: 10.1016/j.bbabio.2006.11.014
22. Gomez A, Chew M, Bryant DA (2007) Chlorophyll biosynthesis in bacteria: the origins of structural and functional diversity. Annual Review of Microbiology 61, 113-129. doi: 10.1146/annurev.micro.61.080 706.093242
23. - pump in Acetabularia membrane by permeability increase for the carrier ion. The Journal of Membrane Biology 44, 1-24. doi: 10.1007/BF01940570
24. Halldal P (1967) Ultraviolet action spectra in algology. A review. Photochemistry and Photobiology 6, 445-460. doi: 10.1111/j.1751-1097.1967.tb08744.x
25. 2-production rate. Journal of Phycology 44, 803-813. doi: 10.1111/j.1529-8817.2008.00509.x
26. Haumann M, Grundmeier A, Zaharieva I, Dau H (2008) Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements. Proceedings of the National Academy of Sciences of the United States of America 105, 17384-17389. doi: 10.1073/pnas.0802596105
27. Hegemann P (2008) Algal sensory photoreceptors. Annual Review of Plant Biology 59, 167-189. doi: 10.1146/annurev.arplant.59.032607.092847
28. Hill R, Bendall F (1960) Function of two cytochrome components in chloroplasts: a working hypothesis. Nature 186, 136-137. doi: 10.1038/186136a0
29. Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (Eds) (1994) 'Bergey's manual of determinative bacteriology, 9th edn.' (Williams and Wilkins: Baltimore)
30. Imasheva ES, Balashov SP, Wang JM, Lanyi JK (2006) pH-dependent transitions in xanthorhodopsin. Photochemistry and Photobiology 82, 1406-1413.
31. Johnsen G, Sakshaug E (2007) Biooptical characteristics of PSII and PSI in 33 species (13 pigment groups) of marine phytoplankton, and the relevance for pulse-amplitude-modulated and fast-repetition-rate fluorometry. Journal of Phycology 43, 1236-1251. doi: 10.1111/j.1529-8817.2007.00422.x
32. Johnson G (2004) Controversy remains: regulation of pH gradient across the thylakoid membrane. Trends in Plant Science 9, 570-571. doi: 10.1016/j.tplants.2004.10.004
33. Kálmán L, LoBrutto R, Allen JP, Williams JC (1999) Modified reaction centres oxidize tyrosine in reactions that mirror photosystem II. Nature 402, 696-699. doi: 10.1038/45300
34. Kálmán L, Williams JC, Allen JP (2008) Comparison of bacterial reaction centers and photosystem II. Photosynthesis Research 98, 643-655. doi: 10.1007/s11120-008-9369-z
35. Kiang NY, Siefert J, Govindjee, Blankenship RE (2007a) Spectral signatures of photosynthesis. I. Review of Earth organisms. Astrobiology 7, 222-251. doi: 10.1089/ast.2006.0105
36. Kiang NY, Segura A, Tinetti G, Govindjee, Blankenship RE, Cohen M, Siefert J, Crisp D, Meadows VS (2007b) Spectral signatures of photosynthesis. II. Coevolution with other stars and the atmosphere on extrasolar worlds. Astrobiology 7, 252-274. doi: 10.1089/ast.2006.0108
37. Kirk JTO (1983) 'Light and photosynthesis in aquatic ecosystems.' (Cambridge University Press: Cambridge)
38. Koenig F, Schmidt M (1995) Gloebacter violaceous - investigation of an unusual photosynthetic apparatus. Absence of the long wavelength emission of photosystem I in 77K fluorescence spectra. Physiologia Plantarum 94, 621-628. doi: 10.1111/j.1399-3054.1995.tb00976.x
39. Kolling DRJ, Brown TS, Ananyev G, Dismukes GC (2009) Photosynthetic oxygen evolution is not reversed by high oxygen pressures: mechanistic consequences for the water-oxidising complex. Biochemistry 48, 1381-1389. doi: 10.1021/bi801774f
40. Koyama K, Suzuki H, Noguchi T, Akimoto S, Tsuchiya T, Mimuro M (2008) Oxygen evolution in the thylakoid-lacking cyanobacterium Gloeobacter violaceous PCC 7421. Biochimica et Biophysica Acta 1777, 369-378. doi: 10.1016/j.bbabio.2008.01.009
41. Kramer DM, Cruz JA, Kanazawa A (2003) Balancing the central roles of the thylakoid proton gradient. Trends in Plant Science 8, 27-32. doi: 10.1016/S1360-1385(02)00010-9
42. Kramer DM, Avenson TJ, Edwards GE (2004) Response to Johnson: controversy remains: regulation of pH gradient across the thylakoid membrane. Trends in Plant Science 9, 571-572. doi: 10.1016/j.tplants.2004.10.005
43. Larkum AWD (2003) Light-harvesting systems in algae. In 'Photosynthesis of Algae'. (Eds AWD Larkum, SE Douglas, JA Raven) pp. 277-304. (Kluwer Academic Publishers: Dordrecht)
44. Larkum AWD (2006) The evolution of chlorophylls and photosynthesis. In 'Chlorophylls and Bacteriochlorophylls. Vol. 25, Advances in Photosynthesis and Respiration'. (Eds B Grimm, RJ Porra, W Rüdiger, H Scheer) pp. 261-282. (Springer-Verlag: Berlin)
45. Larkum AWD (2007) Evolution of the reaction centers and photosystems. In 'Primary Processes of Photosynthesis: Principles and Apparatus. Vol. 2'. (Ed. G Renger) pp. 489-521. (Royal Society of Chemistry: Cambridge)
46. Larkum AWD, Kuhl M (2005) Chlorophyll d: the puzzle resolved. Trends in Plant Science 10, 355-357. doi: 10.1016/j.tplants.2005. 06.005
47. Lüning K (1983) 'Light and photosynthesis in aquatic ecosystems.' (Wiley-Interscience: New York)
48. McCarren J, DeLong EF (2007) Proteorhodopsin photosystem gene clusters exhibit co-evolutionary trends and shared ancestry among diverse marine microbial phyla. Environmental Microbiology 9, 846-858. doi: 10.1111/j.1462-2920.2006.01203.x
49. Mimuro M, Tomo T, Tsuchiya T (2008) Two unique cyanobacteria lead to a traceable approach of the first appearance of oxygenic photosynthesis. Photosynthesis Research 97, 167-176. doi: 10.1007/s11120-008-9311- 4
50. Miranda MRM, Choi AR, Bezerra AH Jr, Jung K-H, Brown LS (2009) The photocycle and proton translocation pathway in a cyanobacterial ion-pumping rhodopsin. Biophysical Journal 96, 1471-1481. doi: 10.1016/j.bpj.2008.11.026
51. Mulkidjanian AY, Junge W (1997) On the origin of photosynthesis as inferred from sequence analysis. A primordial UV-protector as common ancestor of reaction centers and antenna proteins. Photosynthesis Research 51, 27-42. doi: 10.1023/A:1005726809084
52. Nakamura Y, Kaneko T, Sato S, Mimuro M, Miyashita H, et al. (2003) Complete genome structure of Gloeobacter violaceous PCC 7421, a cyanobacterium that lacks thylakoids. DNA Research 10, 137-145. doi: 10.1093/dnares/10.4.137
53. Ohashi S, Miyashita H, Okusa N, Iemura T, Watanabe T, Kobayashi M (2008) Unique photosystems in Acaryochloris marina. Photosynthesis Research 98, 141-149. doi: 10.1007/s11120-008-9383-1
54. Okamoto OK, Hastings JW (2003) Novel dinoflagellate clock-related genes identified through microarray analysis. Journal of Phycology 39, 519-526. doi: 10.1046/j.1529-8817.2003.02170.x
55. Pogoryelov D, Reichen C, Klyszejko AJ, Brunisholz R, Muller DJ, Dimroth P, Meier T (2007) The oligomeric state of c rings from the cyanobacterial F-ATP synthases varies from 13 to 15. Journal of Bacteriology 189, 5895-5902. doi: 10.1128/JB.00581-07
56. Quigg A, Kevekordes K, Raven JA, Beardall J (2006) Limitations on microalgal growth at very low photon fluence rates: the role of energy slippage. Photosynthesis Research 88, 299-310. doi: 10.1007/ s11120-006-9052-1
57. Radmer R, Kok B (1977) Photosynthesis - limited yields, unlimited dreams. American Scientist 27, 599-605.
58. Raven JA (1984a) A cost-benefit analysis of photon absorption by photosynthetic unicells. New Phytologist 98, 593-625. doi: 10.1111/ j.1469-8137.1984.tb04152.x
59. Raven JA (1984b) 'Energetics and transport in aquatic plants.' (A. R. Liss: New York)
60. Raven JA (1987) Biochemistry, biophysics and physiology of chlorophyll b-containing algae: implications for taxonomy and phylogeny. In 'Progress in Phycological Research, Vol. 5'. pp. 1-122. (Biopress Ltd: Bristol, UK)
61. Raven JA (1996) The bigger the fewer: size, taxonomic diversity and the range of pigments in marine phototrophs. Journal of the Marine Biological Association of the United Kingdom 76, 211-217.
62. Raven JA (2007) Photosynthesis in watercolours. Nature 448, 418. doi: 10.1038/448418a
63. Raven JA (2009) Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquatic Microbial Ecology, in press.
64. Raven JA, Larkum AWD (2007) Are there ecological implications for proposed energetic restriction on oxygen evolution at high oxygen concentrations? Photosynthesis Research 94, 31-42. doi: 10.1007/s11120-007-9211-z
65. Raven JA, Wolstencroft RD (2004) Constraints on photosynthesis on Earth and Earth-like planets. Bioastronomy 2002: Life Among the Stars 213, 305-308.
66. 2-evolving organisms. Photosynthesis Research 60, 111-149. doi: 10.1023/A:1006282714942
67. Raven JA, Kübler JE, Beardall J (2000) Put out the light, and then put out the light. Journal of the Marine Biological Association of the United Kingdom 80, 1-25. doi: 10.1017/S0025315499001526
68. Raven JA, Cockell CS, De La Rocha CL (2008) The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 2641-2650. doi: 10.1098/rstb.2008.0020
69. Ruch S, Beyer P, Ernst H, Al-Babili S (2005) Retinal synthesis in Eubacteria: in vitro characterization of a novel carotenoid oxygenase from Synechocystis sp. PCC 6803. Molecular Microbiology 55, 1015-1024. doi: 10.1111/j.1365-2958.2004.04460.x
70. Sabehi G, Kirkup BC, Rozenberg M, Stambler N, Polz MF, Béjà O (2007) Adapation and spectral tuning in divergent marine proteorhodopsins from the eastern Mediterranean and the Sargasso Seas. The ISME Journal 1, 48-55. doi: 10.1038/ismej.2007.10
71. Schilde C (1968) Rapid photoelectric effect in the alga Acetabularia. Zeitschrift für Naturforschung B 23, 1369-1376.
72. Sharma AK, Spudich JL, Doolittle WF (2006) Microbial rhodopsins: functional versatility and genetic mobility. Trends in Microbiology 14, 463-469. doi: 10.1016/j.tim.2006.09.006
73. Sharma AK, Zhaxybayeva O, Papke RT, Doolittle WF (2008) Actinorhodopsins: proteorhodopsin-like gene sequences found predominantly in non-marine environments. Environmental Microbiology 10, 1039-1056. doi: 10.1111/j.1462-2920.2007.01525.x
74. 1-ATPase. Proceedings of the National Academy of Sciences of the United States of America 105, 17 760-17 765. doi: 10.1111/j.1462-2920.2007.01525.x
75. Sineshchekov OA, Govorunova EV (1999) Rhodopsin-mediated photosensing in green flagellated algae. Trends in Plant Science 4, 58-63. doi: 10.1016/S1360-1385(98)01370-3
76. Sineshchekov OA, Govorunova EG, Jung K-H, ZaurerS,Maier UG, Spudich JL (2005) Rhodopsin-mediated photoreceptionincryptophyteflagellates. Biophysical Journal 89, 4310-4319. doi: 10.1529/biophysj.105.070920
77. Spiedel D, Jones MR, Robert B (2002) Tuning of the redox potential of the primary electron donor in reaction centres of purple bacteria: effects of amino acid polarity and position. FEBS Letters 527, 171-175. doi: 10.1016/S0014-5793(02)03203-9
78. +-ATP synthetase from chloroplasts and Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 105, 3745-3750. doi: 10.1073/pnas.0708356105
79. Stomp M, Huisman J, de Jongh F, Veraart AJ, Gerla D, Rijkeboer M, Iberlings BW, Wollenzien UIA, Stal LJ (2004) Adaptive divergence in pigment composition promotes phytoplankton biodiversity. Nature 432, 104-107. doi: 10.1038/nature03044
80. Stomp M, Huisman J, Stal LJ, Matthijs HCP (2007) Colorful niches of phototrophic microorganisms shaped by vibrations of the water molecule. The ISME Journal 1, 271-282.
81. Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431, 689-692. doi: 10.1038/ nature02954
82. Swingley WD, Hohomann-Marriott MF, Olson TL, Blankenship RE (2005) Effect of iron on growth and ultrastructure of Acaryochloris marina. Applied and Environmental Microbiology 71, 8606-8610. doi: 10.1128/AEM.71.12. 8606-8610.2005
83. Terashima I, Fujita T, Inoue T, Chow WS, Oguchi R (2009) Green light drives leaf photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. Plant & Cell Physiology 50, 684-697. doi: 10.1093/pcp/pcp034
84. Ting CS, Rocap G, King J, Chisholm SW (2002) Cyanobacterial photosynthesis in the oceans: the origins and significance of divergent light-harvesting strategies. Trends in Microbiology 10, 134-142. doi: 10.1016/S0966-842X(02)02319-3
85. +-pumping rhodopsin from the marine alga Acetabularia. Biophysical Journal 91, 1471-1479. doi: 10.1529/biophysj.106.086421
86. Wolstencroft D, Raven JA (2002) Photosynthesis: likelihood of occurrence and possibility of detection in Earth-like planets. Icarus 157, 535-548. doi: 10.1006/icar.2002.6854
87. Wood AM (1985) Adaptation of the photosynthetic apparatus of marine phytoplankton to natural light fields. Nature 316, 253-255. doi: 10.1038/316253a0
88. 2-fixing cyanobacteria lack oxygenic photosystem II. Science 322, 1110-1112. doi: 10.1126/ science.1165340