Photosynthesis in Chromera velia Represents a Simple System with High Efficiency

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Quigg, Antonietta ^a,b   Kotabová, Eva ^c,d   Jarešová, Jana ^c,d   Kaňa, Radek ^c,d   Šetlík, Jiří ^c   Šedivá, Barbora ^c   Komárek, Ondřej ^c   Prášil, Ondřej ^c,d  

^a TEXAS A AND M UNIVERSITY AT GALVESTON   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c INSTITUTE OF MICROBIOLOGY   (Czech Republic)

^d UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; CAROTENOID; CHLOROPHYLL; OXYGEN;

ALVEOLATA; ARTICLE; CARBON FIXATION; CHROMERA VELIA; CONTROLLED STUDY; FLUORESCENCE SPECTROSCOPY; GAS EXCHANGE; LIGHT DARK CYCLE; LIGHT IRRADIANCE; NONHUMAN; NONPHOTOCHEMICAL QUENCHING; PHOTOINHIBITION; PHOTORESPIRATION; PHOTOSYNTHESIS; PHOTOSYSTEM II;

ACCLIMATIZATION; ALVEOLATA; CARBON RADIOISOTOPES; CAROTENOIDS; CHLOROPHYLL; FLUORESCENCE; OXYGEN; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 84867378262     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047036     Document Type: Article

References (70)

1. Quigg A, Finkel ZV, Irwin AJ, Reinfelder JR, Rosenthal Y, et al. (2003) The evolutionary inheritance of elemental stoichiometry in marine phytoplankton. Nature 425: 291-294.
2. Quigg A, Irwin AJ, Finkel ZV, (2011) Evolutionary imprint of endosymbiosis of elemental stoichiometry: testing inheritance hypotheses. Proc R Soc Lond: B 278: 526-534.
3. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, et al. (2004) The evolution of modern eukaryotic phytoplankton. Science 305: 354-360.
4. McFadden GI, Waller RE, Reith ME, Langunnasch N, (1997) Plastids in apicomplexan parasites. Plant System Evol 11: 261-287.
5. Ralph SA, van Dooren GG, Waller RF, Crawford MJ, Fraunholz MJ, et al. (2004) Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat Rev Microbiol 2: 203-216.
6. Oborník M, Modrý D, Lukeš M, Černotíková-Stříbrná E, Cihlář J, et al. (2012) Morphology, ultrastructure and life cycle of Vitrella brassicaformis n. sp., n. gen., a novel chromerid from the Great Barrier Reef. Protist 163: 306-323.
7. Cavalier-Smith T, (1999) Principles of protein and lipid targeting in secondary symbiogenesis: Euglenoid, dinoflagellate, and sporozoan plastid origins and theeukaryote family tree. J Eukaryot Microbiol 46: 347-366.
8. Cavalier-Smith T (2004) Chromalveolate diversity and cell megaevolution: interplay of membranes, genomes and cytoskeleton. In: Hirt RP, Horner D, editors. Organelles, genomes and eukaryotic evolution. Taylor and Francis, London. pp. 71-103.
9. Keeling PJ, (2009) Chromalveolates and the evolution of plastids by secondary endosymbiosis. J Eukaryot Microbiol 56: 1-8.
10. Moore RB, Oborník M, Janouškovec J, Chrudimský T, Vancová M, et al. (2008) A photosynthetic alveolate closely related to apicomplexan parasites. Nature 451: 959-963.
11. Zhang Z, Green BR, Cavalier-Smith T, (2000) Phylogeny of ultra-rapidly evolving dinoflagellate chloroplast genes: A possible common origin for sporozoan and dinoflagellate plastids. J Mol Evol 51: 26-40.
12. Fast NM, Kissinger JC, Roos DS, Keeling PJ, (2001) Nuclear-encoded, plastid targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol Biol Evol 18: 418-426.
13. Kořený L, Sobotka R, Janouškovec J, Keeling PJ, Oborník M, (2011) Tetrapyrrole synthesis of photosynthetic chromerids is likely homologous to the unusual pathway of apicomplexan parasites. Plant Cell 23: 3454-3462.
14. Chang SS, Prézelin BB, Trench RK, (1983) Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar Biol 76: 219-229.
15. Muscatine L, Falkowski PG, Porter JW, Dubinsky Z, (1984) Fate of photosynthetic fixed carbon in light-adapted and shade-adapted colonies of the symbiotic coral Stylophora pistillata. Proc R Soc Lond B 222: 181-202.
16. Yellowlees D, Warner M (2003) Photosynthesis in symbiotic algae. In: Larkum AWD, Douglas SE, Raven JA, editors. Photosynthesis in Algae. Advances in Photosynthesis and Respiration. Springer. pp. 437-455.
17. Sheppard CRC, Davy SK, Pilling GM (2009) The Biology of Coral Reefs. The Biology of Habitats Series, Oxford University Press. 352 p.
18. Oborník M, Janouskovec J, Chrudimský T, Lukes J, (2009) Evolution of the apicoplast and its hosts: From heterotrophy to autotrophy and back again. Int J Parasitol 39: 1-12.
19. Janouškovec J, Horák A, Oborník M, Lukes J, Keeling PJ, (2010) A common red algal origin of the apicomplexan, dinoflagellate, and heterokont plastids. Proc Natl Acad Sci U.S.A 107: 10949-10954.
20. Okamoto N, McFadden GI, (2008) The mother of all parasites. Future Microbiol 3: 391-395.
21. Oborník M, Vancová M, Lai DH, Janouškovec J, Keeling PJ, et al. (2011) Morphology and ultrastructure of multiple life cycle stages of the photosynthetic relative of apicomplexa, Chromera velia. Protist 162: 115-130.
22. Weatherby K, Murray S, Carter DJ, Šlapeta J, (2011) Surface and flagella morphology of the motile form of Chromera velia revealed by field-emission scanning electron microscopy. Protist 162: 142-153.
23. Sutak R, Šlapeta J, San Roman M, Camadro J-M, Lesuisse E, (2010) Nonreductive iron uptake mechanism in the marine alveolate Chromera velia. Plant Physiol 154: 991-1000.
24. Guo JT, Weatherby K, Carter D, Šlapeta J, (2010) Effect of nutrient concentration and salinity on immotile-motile transformation of Chromera velia. J Eukaryot Microbiol 57: 444-446.
25. Kotabová E, Kaňa R, Jarešová J, Prášil O, (2011) Non-photochemical fluorescence quenching in Chromera velia is enabled by fast violaxanthin de-epoxidation. Febs Letters 585: 1941-1945.
26. Pan H, Šlapeta J, Carter D, Chen M, (2012) Phylogenetic analysis of the light-harvesting system in Chromera velia. Photosyn Res 111: 19-28.
27. Botté CY, Yamaryo-Botté Y, Janouškovec J, Rupasinghe T, Keeling PJ, et al. (2011) Identification of plant-like galactolipids in Chromera velia, a photosynthetic relative of malaria parasites. J Biol Chem 286: 29893-29903.
28. Leblond JD, Dodson J, Khadka M, Holder S, Seipelt RL, (2012) Sterol Composition and Biosynthetic Genes of the Recently Discovered Photosynthetic Alveolate, Chromera velia (Chromerida), a Close Relative of Apicomplexans. J. Eukaryot. Microbiol 0 (0):: 1-7 DOI: 10.1111/j.1550-7408.2012.00611.x.
29. Havelková-Doušová H, Prášil O, Behrenfeld MJ, (2004) Photoacclimation of Dunaliella tertiolecta (Chlorophyceae) under fluctuating irradiance. Photosynthetica 42: 273-281.
30. Jeffrey SW, Vesk M (1997) Introduction to marine phytoplankton and their pigment signatures. In: Jeffrey SW, Mantoura RFC, Wright SW, editors. Phytoplankton pigments in oceanography. Paris: UNESCO Publishing. pp 37-84.
31. Porra RJ, Thompson WA, Kriedemann PE, (1989) determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: Verification of the concentration of chlorophyll standards by atomic absorption spectrometry. Biochim Biophys Acta 975: 384-394.
32. Kaňa R, Kotabová E, Komárek O, Papageorgiou GC, Govindjee, et al, (2012a) Slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim Biophys Acta in press.
33. Kolber ZS, PrasilO, Falkowski PG, (1998) Measurements of variable chlorophyll fluorescence using fast repetition rate techniques: defining methodology and experimental protocols. Biochim Biophys Acta 1367: 88-106.
34. Suggett DJ, Moore CM, Geider RJ (2010) Estimating Aquatic Productivity from Active Fluorescence Measurement. In: Suggett DJ, Prasil O, Borowitzka M.A, editors. Chlorophyll a Fluorescence in Aquatic Sciences: Methods and Applications. Springer, Dordrecht, pp 103-127.
35. Lewis MR, Smith JC, (1983) A small volume, short-incubation-time method for measurement of photosynthesis as a function of incident irradiance. Mar Ecol Prog Ser 13: 99-102.
36. Butler NB (1982) Carbon dioxide equilibria and their applications. New York: Addison-Wesley Publishing Company Inc. 259 p.
37. Jassby AD, Platt T, (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21: 540-547.
38. Falkowski PG, Dubinsky Z, Wyman K, (1985a) Growth-irradiance relationships in phytoplankton. Limnol Oceanogr 30: 311-321.
39. Falkowski PG, Dubinsky Z, Santostefano G, (1985b) Light-enhanced dark respiration in phytoplankton. Verh Internat Verein Limnol 22: 2830-2833.
40. Levy O, Dubinsky Z, Schneider K, Achituv Y, Zakai D, et al. (2004) Diurnal hysteresis in coral photosynthesis. Mar Ecol Prog Ser 268: 105-117.
41. Falkowski PG, Dubinsky Z, Muscatine L, Porter JW, (1984) Light and bioenergetics of symbiotic coral. BioScience 34: 705-709.
42. Porter JW, Muscatine L, Dubinsky Z, Falkowski PG, (1984) Primary production and photoadaptation in light-adapted and shade-adapted colonies of the symbiotic coral, Stylophora pistillata. Proc R Soc Lond B 222: 161-180.
43. Gorbunov MY, Falkowski PG, Kolber ZS, (2000) Measurement of photosynthetic parameters in benthic organisms in situ using a SCUBA-based fast repetition rate fluorometer. Limnol Oceanogr 45: 242-245.
44. Gorbunov MY, Kolber ZS, Lesser MP, Falkowski PG, (2001) Photosynthesis and photoprotection in symbiotic corals. Limnol Oceanogr 46: 75-85.
45. Hennige SJ, Suggett DJ, Warner ME, McDougall KE, Smith DJ, (2009) Photobiology of Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28: 179-195.
46. Hoegh-Guldberg O, Jones R, (1999) Photoinhibition and photoprotection in symbiotic dinoflagellates from reef-building corals. Mar Ecol Prog Ser 183: 73-86.
47. Jones RJ, Hoegh-Guldberg O, (2001) Diurnal changes in the photochemical efficiency of the symbiotic dinoflagellates (Dinophyceae) of corals: photoprotection, photoinactivation and the relationship to coral bleaching. Plant Cell Environ 24: 89-99.
48. Ralph PJ, Gademann R, Larkum AWD, Kahl M, (2002) Spatial heterogeneity in active chlorophyll fluorescence and PSII activity of coral tissues. Mar Biol 141: 639-646.
49. Ragni M, Airs RL, Hennige SJ, Suggett DJ, Warner ME, et al. (2010) PSII photoinhibition and photorepair of Symbiodinium (Pyrrophyta) differs between thermally tolerant and sensitive phylotypes. Mar Ecol Prog Ser 406: 57-70.
50. Suggett DJ, Warner M, Smith DJ, Davey P, Hennige S, et al. (2008) Photosynthesis and production of hydrogen peroxide by symbiotic dinoflagellates during short-term heat stress. J Phycol 44: 948-956.
51. Iglesias-Prieto R, Beltran V, La Jeunesse T, Reyes-Bonilla H, Thome P, (2004) Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Lond B 271: 1757-1763.
52. Hoegh-Guldberg O, Mumby PJ, Hooten AJ, (2007) Coral reefs under rapid climate change and ocean acidification. Science 318: 739-742.
53. Quigg A, Beardall J, (2003) Protein turnover in relation to maintenance metabolism at low photon flux in two marine microalgae. Plant, Cell Environ 26: 1-10.
54. Warner ME, Lesser MP, Ralph PJ (2010) Chlorophyll fluorescence in reef building corals. In: Suggett DJ, Prášil O, Borowitzka M, editors. Chlorophyll Fluorescence in Aquatic Sciences: Methods and Applications. Springer. pp. 209-222.
55. Kaňa R, Kotabová E, Sobotka R, Prášil O, (2012b) Non-photochemical quenching in cryptophyte alga Rhodomona ssalina is located in chlorophyll a/c antennae. PLoS One 7: e29700.
56. Prášil O, Adir N, Ohad I (1992) Dynamics of Photosystem II: mechanism of photoinhibition and recovery processes. In: Barber J, editor. The Photosystems: Structure, Function and Molecular Biology. Elsevier Science, Oxford. pp. 295-348.
57. Kaňa R, Lazar D, Prášil O, Naus J, (2002) Experimental and theoretical studies on the excess capacity of Photosystem II. Photosyn Res 72: 271-284.
58. Beardall J, Quigg A, Raven JA (2003) Oxygen consumption: Photorespiration and chlororespiration. In: Larkum AWD, Douglas SE, Raven JA, editors. Photosynthesis in Algae. Advances in Photosynthesis and Respiration. Springer. pp. 157-181.
59. Crawley A, Kline DI, Dunn S, Anthony K, Dove S, (2010) The effect of ocean acidification on symbiont photorespiration and productivity in Acropora formosa. Global Change Biol 16: 851-863.
60. Nassoury N, Fritz L, Morse D, (2001) Circadian changes in ribulose-1,5-bisphosphate carboxylase/oxygenase distribution inside individual chloroplasts can account for the rhythm in dinoflagellate carbonfixation. Plant Cell 13: 923-934.
61. Leggat W, Badger M, Yellowlees D, (1999) Evidence for an inorganic carbon-concentrating mechanism in the symbiotic dinoflagellate Symbiodinium sp. Plant Physiol 121: 1247-1255.
62. Burris JE, (1981) Effects of oxygen and inorganic carbon concentrations on the photosynthetic quotients of marine algae. Mar Biol 65: 215-219.
63. Whitney SM, Andrews TJ, (1998) The CO2/O2 specificity of single-subunit ribulose-bisphosphate carboxylase from the dinoflagellate, Amphidinium carterae. Aus J Plant Physiol 25: 131-138.
64. Badger MR, Bek EJ, (2008) Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot 59: 1525-1541.
65. Schnepf E, Elbrachter M, (1999) Dinophyte chloroplasts and phylogeny- A review. GRANA 38: 81-97.
66. Mehler AH, (1957) Studies on reactions of illuminated chloroplasts, I: Mechanism of the reduction of oxygen and other Hill reagents. Arch BiochemBiophys 33: 65-77.
67. Peltier G, Cournac L, (2002) Chlororespiration. Ann Rev Plant Physiol Plant Mol Biol 53: 523-550.
68. Peltier G, Tolleter D, Billon E, Cournac L, (2010) Auxiliary electron transport pathways in chloroplasts of microalgae. Photosyn Res 106: 19-31.
69. Reynolds JM, Bruns BU, Fitt WK, Schmidt GW, (2008) Enhanced photoprotection pathways in symbiotic dinoflagellates of shallow-water corals and other cnidarians. Proc Natl Acad Sci U.S.A 105: 13674-13678.
70. Cardol P, Forti G, Finazzi G, (2011) Regulation of electron transport in microalgae. Biochim Biophys Acta 1807: 912-918.