Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
EVOLUTIONARY REVIEW

Functional evolution of photochemical energy transformations in oxygen-producing organisms

John A. Raven
+ Author Affiliations
- Author Affiliations

A Division of Plant Sciences, University of Dundee at SCRI, Invergowrie, Dundee DD2 5DA, UK. Email: j.a.raven@dundee.ac.uk

This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.

Functional Plant Biology 36(6) 505-515 https://doi.org/10.1071/FP09087
Submitted: 6 April 2009  Accepted: 21 April 2009   Published: 1 June 2009

Abstract

Chlorophyll a is the photochemical agent accounting for most oxygenic photosynthesis, that is, over 99.9% of photosynthetic primary activity on Earth. The spectral and energetic properties of chlorophyll a can, at least in part, be rationalised in terms of the solar spectral output and the energetics of oxygen production and carbon dioxide reduction with two photochemical reactions. The long wavelength limit on in vivo chlorophyll a absorption is probably close to the energetic limit: longer wavelengths could not support a high rate and efficiency of oxygenic photosynthesis. Retinal, a β-carotene derivative that is the chromophore of rhodopsin, acts not only as a sensory pigment, but also as an ion-pumping photochemical transducer. Both sensory and energy-transforming rhodopsins occur in oxygenic phototrophs, although the extent of expression and the function of the latter are not well understood.

Additional keywords: chlorophyll a, photosynthesis, retinal.


Acknowledgements

Discussions with John Beardall, Charles Cockell, Paul Falkowski, Kevin Flynn, Richard Geider, Mario Giordano and Tony Larkum were very helpful. This paper was significantly improved by comments on an earlier version from Tony Larkum and from two anonymous reviewers. The University of Dundee is a registered Scottish charity (No: SC015096).


References


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)

Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends in Plant Science 8, 15–19.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Allen JF (2004) Cytochrome b6f: structure for signalling and vectorial metabolism. Trends in Plant Science 9, 130–137.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Allen JF (2005) A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Letters 579, 963–968.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Allen JF, Martin W (2007) Out of thin air. Nature 445, 610–612.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
CAS | PubMed |
open url image1

Belkin S, Mehlhorn RJ, Packer L (1987) Proton gradients in intact cyanobacteria. Plant Physiology 84, 25–30.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Beust H, Bonfils X, Delfosse X, Udry S (2008) Dynamical evolution of the Gliese 581 planetary system. Astronomy & Astrophysics 479, 277–282.
Crossref | GoogleScholarGoogle Scholar | open url image1

Björn LO, Papageorgiou GC, Blankenship RE, Govindjee (2009) A viewpoint: why chlorophyll a? Photosynthesis Research 99, 85–98.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bryant DA, Friggard N-U (2006) Prokaryotic photosynthesis and phototrophy illuminated. Trends in Microbiology 14, 488–496.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Clausen J, Junge W (2008a) The terminal reaction cascade of water oxidation: proton and oxygen release. Biochimica et Biophysica Acta 1777, 1311–1318.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Clausen J, Junge W (2008b) The inhibitory effects of acidification and augmentated oxygen pressure on water oxidation. Photosynthesis Research 98, 229–233.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Clausen J, Junge W, Dau H, Haumann M (2005) Photosynthetic water oxidation at high O2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry 44, 12775–12779.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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. open url image1

Duyens LNM (1956) The flattening of the absorption of suspensions, as compared to that of solutions. Biochimica et Biophysica Acta 19, 1–12.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Engelmann TW (1883) Farbe und assimilation. Botanische Zeitung 41, 1–29. open url image1

Falkowski PG , Raven JA (2007) ‘Aquatic photosynthesis, 2nd edn’. (Princeton University Press: Princeton)

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gradmann D (1978) Green light (550 nm) inhibits electrogenic Cl− pump in Acetabularia membrane by permeability increase for the carrier ion. The Journal of Membrane Biology 44, 1–24.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Halldal P (1967) Ultraviolet action spectra in algology. A review. Photochemistry and Photobiology 6, 445–460.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hancke TB, Hancke K, Johnsen G, Sakshaug E (2008) Rate of O2 production derived from pulse-amplitude-modulated fluorescence: testing three biooptical approaches against measured O2-production rate. Journal of Phycology 44, 803–813.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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, 17 384–17 389.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hegemann P (2008) Algal sensory photoreceptors. Annual Review of Plant Biology 59, 167–189.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Hill R, Bendall F (1960) Function of two cytochrome components in chloroplasts: a working hypothesis. Nature 186, 136–137.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Holt JG , Krieg NR , Sneath PHA , Staley JT , Williams ST (Eds) (1994) ‘Bergey’s manual of determinative bacteriology, 9th edn.’ (Williams and Wilkins: Baltimore)

Imasheva ES, Balashov SP, Wang JM, Lanyi JK (2006) pH-dependent transitions in xanthorhodopsin. Photochemistry and Photobiology 82, 1406–1413.
CAS | PubMed |
open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Johnson G (2004) Controversy remains: regulation of pH gradient across the thylakoid membrane. Trends in Plant Science 9, 570–571.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kálmán L, LoBrutto R, Allen JP, Williams JC (1999) Modified reaction centres oxidize tyrosine in reactions that mirror photosystem II. Nature 402, 696–699.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kálmán L, Williams JC, Allen JP (2008) Comparison of bacterial reaction centers and photosystem II. Photosynthesis Research 98, 643–655.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kiang NY, Siefert J, Govindjee , Blankenship RE (2007a) Spectral signatures of photosynthesis. I. Review of Earth organisms. Astrobiology 7, 222–251.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kirk JTO (1983) ‘Light and photosynthesis in aquatic ecosystems.’ (Cambridge University Press: Cambridge)

Koenig F, Schmidt M (1995) Gloebacter violaceous – investigation of an unusual photosynthetic apparatus. Absence of the long wavelength emission of photosystem I in 77 K fluorescence spectra. Physiologia Plantarum 94, 621–628.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Kramer DM, Cruz JA, Kanazawa A (2003) Balancing the central roles of the thylakoid proton gradient. Trends in Plant Science 8, 27–32.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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)

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)

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)

Larkum AWD, Kuhl M (2005) Chlorophyll d: the puzzle resolved. Trends in Plant Science 10, 355–357.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Lüning K (1983) ‘Light and photosynthesis in aquatic ecosystems.’ (Wiley-Interscience: New York)

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Miranda MRM, Choi AR, Bezerra AH, Jung K-H, Brown LS (2009) The photocycle and proton translocation pathway in a cyanobacterial ion-pumping rhodopsin. Biophysical Journal 96, 1471–1481.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Ohashi S, Miyashita H, Okusa N, Iemura T, Watanabe T, Kobayashi M (2008) Unique photosystems in Acaryochloris marina. Photosynthesis Research 98, 141–149.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Okamoto OK, Hastings JW (2003) Novel dinoflagellate clock-related genes identified through microarray analysis. Journal of Phycology 39, 519–526.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Radmer R, Kok B (1977) Photosynthesis – limited yields, unlimited dreams. American Scientist 27, 599–605. open url image1

Raven JA (1984a) A cost-benefit analysis of photon absorption by photosynthetic unicells. New Phytologist 98, 593–625.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Raven JA (1984 b) ‘Energetics and transport in aquatic plants.’ (A. R. Liss: New York)

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)

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.
Crossref |
open url image1

Raven JA (2007) Photosynthesis in watercolours. Nature 448, 418.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Raven JA (2009) Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquatic Microbial Ecology in press , open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Raven JA, Wolstencroft RD (2004) Constraints on photosynthesis on Earth and Earth-like planets. Bioastronomy 2002: Life Among the Stars 213, 305–308.
CAS |
open url image1

Raven JA, Evans MCW, Korb RE (1999) The role of trace metals in photosynthetic electron transport in O2-evolving organisms. Photosynthesis Research 60, 111–149.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Schilde C (1968) Rapid photoelectric effect in the alga Acetabularia. Zeitschrift für Naturforschung B 23, 1369–1376.
CAS |
open url image1

Sharma AK, Spudich JL, Doolittle WF (2006) Microbial rhodopsins: functional versatility and genetic mobility. Trends in Microbiology 14, 463–469.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sielaff M, Rennekamp H, Wächter A, Xie H, Hilbers F, Feldbauer K, Dunn SD, Engelbrecht S, Junge W (2008) Domain compliance and elastic power transmission in rotary F0F1-ATPase. Proceedings of the National Academy of Sciences of the United States of America 105, 17 760–17 765.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Sineshchekov OA, Govorunova EV (1999) Rhodopsin-mediated photosensing in green flagellated algae. Trends in Plant Science 4, 58–63.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sineshchekov OA, Govorunova EG, Jung K-H, Zaurer S, Maier UG, Spudich JL (2005) Rhodopsin-mediated photoreception in cryptophyte flagellates. Biophysical Journal 89, 4310–4319.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Steigmiller S, Turina P, Gräber P (2008) The thermodynamic H+/ATP ratios of the H+-ATP synthetase from chloroplasts and Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 105, 3745–3750.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
CAS | PubMed |
open url image1

Strzepek RF, Harrison PJ (2004) Photosynthetic architecture differs in coastal and oceanic diatoms. Nature 431, 689–692.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

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.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Tsunoda SP, Ewers D, Gazzarrini S, Motoni A, Gradmann D, Hegemann P (2006) H+-pumping rhodopsin from the marine alga Acetabularia. Biophysical Journal 91, 1471–1479.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1

Wolstencroft D, Raven JA (2002) Photosynthesis: likelihood of occurrence and possibility of detection in Earth-like planets. Icarus 157, 535–548.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Wood AM (1985) Adaptation of the photosynthetic apparatus of marine phytoplankton to natural light fields. Nature 316, 253–255.
Crossref | GoogleScholarGoogle Scholar | CAS | open url image1

Zehr JP, Bench SR, Crater BJ, Hewson I, Niazi F, Shi T, Tripp HJ, Affourtit JP (2008) Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II. Science 322, 1110–1112.
Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | open url image1