Rising CO2 Interacts with Growth Light and Growth Rate to Alter Photosystem II Photoinactivation of the Coastal Diatom Thalassiosira pseudonana

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Li, Gang ^a,b   Campbell, Douglas A ^a  

^a MOUNT ALLISON UNIVERSITY   (Canada)

^b SOUTH CHINA SEA INSTITUTE OF OCEANOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON DIOXIDE; CARBONIC ACID; CELL PROTEIN; CHLOROPHYLL A; MALONALDEHYDE; MICROORGANISM PROTEIN; NITROGEN; PROTEIN PSAC; PROTEIN RBCL; UNCLASSIFIED DRUG; CARBON; CARBONIC ACID DERIVATIVE; SEA WATER;

ARTICLE; CARBON DIOXIDE TENSION; CELL VOLUME; CONTROLLED STUDY; GROWTH RATE; LIGHT INTENSITY; LIPID PEROXIDATION; MARINE SPECIES; MICROBIAL GROWTH; MOLECULAR INTERACTION; NONHUMAN; PHOTOCHEMISTRY; PHOTODYNAMICS; PHOTOINACTIVATION; PHOTON; PHOTOSYSTEM II; THALASSIOSIRA PSEUDONANA; CHEMISTRY; DIATOM; GROWTH, DEVELOPMENT AND AGING; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PROTEIN SUBUNIT;

CARBON; CARBON DIOXIDE; CARBONATES; DIATOMS; LIGHT; LIPID PEROXIDATION; MALONDIALDEHYDE; NITROGEN; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PROTEIN SUBUNITS; SEAWATER;

MLCS; MLOWN;

EID: 84873120731     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055562     Document Type: Article

References (82)

1. Intergovernmental Panel on Climate Change (2007) Climate change 2007: mitigation of climate change: contribution of Working Group III to the Fourth assessment report of the Intergovernmental Panel on Climate Change. Cambridge: Cambridge University Press. 851 p.
2. Zeebe RE, Zachos JC, Caldeira K, Tyrrell T, (2008) Carbon Emissions and Acidification. Science 321: 51-52 doi:10.1126/science.1159124.
3. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, et al. (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437: 681-686 doi:10.1038/nature04095.
4. Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, et al. (2010) The Effect of Ocean Acidification on Calcifying Organisms in Marine Ecosystems: An Organism-to-Ecosystem Perspective. Annual Review of Ecology, Evolution, and Systematics 41: 127-147 doi:10.1146/annurev.ecolsys.110308.120227.
5. Hopkinson BM, Dupont CL, Allen AE, Morel FMM, (2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proceedings of the National Academy of Sciences 108: 3830-3837 doi:10.1073/pnas.1018062108.
6. Raven JA, Giordano M, Beardall J, Maberly SC, (2012) Algal evolution in relation to atmospheric CO2: carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 493-507 doi:10.1098/rstb.2011.0212.
7. Wu Y, Gao K, Riebesell U, (2010) CO2-induced seawater acidification affects physiological performance of the marine diatom Phaeodactylum tricornutum. Biogeosciences 7: 2915-2923 doi:10.5194/bg-7-2915-2010.
8. McCarthy A, Rogers SP, Duffy SJ, Campbell DA, (2012) Elevated carbon dioxide differentially alters the photophysiology of Thalassiosira pseudonana (Bacillariophyceae) and Emiliana huxleyi (Haptophyta). Journal of Phycology 48: 635-646 doi:10.1111/j.1529-8817.2012.01171.x.
9. Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, et al. (1998) The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Canadian Journal of Botany 76: 1052-1071 doi:10.1139/b98-074.
10. Schippers P, Lürling M, Scheffer M, (2004) Increase of atmospheric CO2 promotes phytoplankton productivity. Ecology Letters 7: 446-451 doi:10.1111/j.1461-0248.2004.00597.x.
11. Crawfurd KJ, Raven JA, Wheeler GL, Baxter EJ, Joint I, (2011) The Response of Thalassiosira pseudonana to Long-Term Exposure to Increased CO2 and Decreased pH. PLoS ONE 6: e26695 doi:10.1371/journal.pone.0026695.
12. Low-Décarie E, Fussmann GF, Bell G, (2011) The effect of elevated CO2 on growth and competition in experimental phytoplankton communities. Global Change Biology 17: 2525-2535 doi:10.1111/j.1365-2486.2011.02402.x.
13. Hare CE, Leblanc K, DiTullio GR, Kudela RM, Zhang Y, et al. (2007) Consequences of increased temperature and CO2 for phytoplankton community structure in the Bering Sea. Marine Ecology Progress Series 352: 9-16 doi:10.3354/meps07182.
14. Yoshimura T, Nishioka J, Suzuki K, Hattori H, Kiyosawa H, et al. (2009) Impacts of elevated CO2 on phytoplankton community composition and organic carbon dynamics in nutrient-depleted Okhotsk Sea surface waters. Biogeosciences Discussions 6: 4143-4163 doi:10.5194/bgd-6-4143-2009.
15. Feng Y, Hare CE, Rose JM, Handy SM, DiTullio GR, et al. (2010) Interactive effects of iron, irradiance and CO2 on Ross Sea phytoplankton. Deep Sea Research Part I: Oceanographic Research Papers 57: 368-383 doi:10.1016/j.dsr.2009.10.013.
16. Gao K, Xu J, Gao G, Li Y, Hutchins DA, et al. (2012) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nature Climate Change 2: 519-523 doi:10.1038/nclimate1507.
17. Boyd PW, Strzepek R, Fu F, Hutchins DA, (2010) Environmental control of open-ocean phytoplankton groups: Now and in the future. Limnology and Oceanography 55: 1353-1376 doi:10.4319/lo.2010.55.3.1353.
18. Yang G, Gao K, (2012) Physiological responses of the marine diatom Thalassiosira pseudonana to increased pCO2 and seawater acidity. Marine Environmental Research 79: 142-151 doi:10.1016/j.marenvres.2012.06.002.
19. Boelen P, Van de Poll WH, Van der Strate HJ, Neven IA, Beardall J, et al. (2011) Neither elevated nor reduced CO2 affects the photophysiological performance of the marine Antarctic diatom Chaetoceros brevis. Journal of Experimental Marine Biology and Ecology 406: 38-45 doi:10.1016/j.jembe.2011.06.012.
20. Nielsen LT, Hallegraeff GM, Wright SW, Hansen PJ, (2012) Effects of experimental seawater acidification on an estuarine plankton community. Aquatic Microbial Ecology 65: 271-285 doi:10.3354/ame01554.
21. Tortell PD, DiTullio GR, Sigman DM, Morel FMM, (2002) CO2 effects on taxonomic composition and nutrient utilization in an Equatorial Pacific phytoplankton assemblage. Marine Ecology Progress Series 236: 37-43 doi:10.3354/meps236037.
22. Falkowski PG, Owens TG, Ley AC, Mauzerall DC, (1981) Effects of Growth Irradiance Levels on the Ratio of Reaction Centers in Two Species of Marine Phytoplankton 1. Plant Physiology 68: 969-973.
23. Leonardos N, Geider RJ, (2004) Effects of nitrate: phosphate supply ratio and irradiance on the C: N: P stoichiometry of Chaetoceros muelleri. European Journal of Phycology 39: 173-180 doi:10.1080/0967026042000201867.
24. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI, (2007) Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta 1767: 414-421 doi:10.1016/j.bbabio.2006.11.019.
25. Raven JA, (2011) The cost of photoinhibition. Physiologia Plantarum 142: 87-104 doi:10.1111/j.1399-3054.2011.01465.x.
26. Moore JK, Doney SC, Glover DM, Fung IY, (2001) Iron cycling and nutrient-limitation patterns in surface waters of the World Ocean. Deep Sea Research Part II: Topical Studies in Oceanography 49: 463-507 doi:10.1016/S0967-0645(01)00109-6.
27. Sarthou G, Timmermans KR, Blain S, Tréguer P, (2005) Growth physiology and fate of diatoms in the ocean: a review. Journal of Sea Research 53: 25-42 doi:10.1016/j.seares.2004.01.007.
28. Wagner H, Jakob T, Wilhelm C, (2006) Balancing the energy flow from captured light to biomass under fluctuating light conditions. The New Phytologist 169: 95-108 doi:10.1111/j.1469-8137.2005.01550.x.
29. Lavaud J (2007) Fast regulation of photosynthesis in diatoms: mechanisms, evolution and ecophysiology. In: Functional Plant Science and Biotechnology. Ikenobe, Japan: Global Science Books. pp. 267-287.
30. Lavaud J, Strzepek RF, Kroth PG, (2007) Photoprotection capacity differs among diatoms: Possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate. Limnology and Oceanography 52: 1188-1194 doi:10.4319/lo.2007.52.3.1188.
31. Key T, McCarthy A, Campbell DA, Six C, Roy S, et al. (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environmental Microbiology 12: 95-104.
32. Loebl M, Cockshutt AM, Campbell DA, Finkel ZV, (2010) Physiological basis for high resistance to photoinhibition under nitrogen depletion in Emiliania huxleyi. Limnology and Oceanography 55: 2150-2160 doi:10.4319/lo.2010.55.5.2150.
33. Ragni M, Airs R, Leonardos N, Geider R, (2008) Photoinhibition of PSII in Emiliania huxleyi (Haptophyta) under high light stress: The roles of photoacclimation, photoprotection and photorepair. Journal of Phycology 44: 670-683 doi:10.1111/j.1529-8817.2008.00524.x.
34. Six C, Finkel ZV, Irwin AJ, Campbell DA, (2007) Light Variability Illuminates Niche-Partitioning among Marine Picocyanobacteria. PLoS ONE 2: e1341 doi:10.1371/journal.pone.0001341.
35. Six C, Sherrard R, Lionard M, Roy S, Campbell DA, (2009) Photosystem II and Pigment Dynamics among Ecotypes of the Green Alga Ostreococcus. Plant Physiology 151: 379-390.
36. Quigg A, Beardall J, (2003) Protein turnover in relation to maintenance metabolism at low photon flux in two marine microalgae. Plant, Cell & Environment 26: 693-703 doi:10.1046/j.1365-3040.2003.01004.x.
37. Hoogstraten A, Timmermans KR, De Baar HJW, (2012) Morphological and physiological effects in Proboscia alata (Bacillariophyceae) grown under different light and CO2 conditions of the modern southern ocean. Journal of Phycology 48: 559-568 doi:10.1111/j.1529-8817.2012.01148.x.
38. Armbrust EV, Berges JA, Bowler C, Green BR, Martinez D, et al. (2004) The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306: 79-86 doi:10.1126/science.1101156.
39. Grouneva I, Rokka A, Aro E-M, (2011) The thylakoid membrane proteome of two marine diatoms outlines both diatom-specific and species-specific features of the photosynthetic machinery. Journal of Proteome Research 10: 5338-5353 doi:10.1021/pr200600f.
40. Li G, Gao K, Yuan D, Zheng Y, Yang G, (2011) Relationship of photosynthetic carbon fixation with environmental changes in the Jiulong River estuary of the South China Sea, with special reference to the effects of solar UV radiation. Marine Pollution bulletin 62: 1852-1858 doi:10.1016/j.marpolbul.2011.02.050.
41. Zhai W, Dai M, Cai W-J, Wang Y, Wang Z, (2005) High partial pressure of CO2 and its maintaining mechanism in a subtropical estuary: the Pearl River estuary, China. Marine Chemistry 93: 21-32 doi:10.1016/j.marchem.2004.07.003.
42. Berges JA, Franklin DJ, Harrison PJ, (2001) Evolution of an artificial seawater medium: Improvements in enriched seawater, artificial water over the last two decades. Journal of Phycology 37: 1138-1145 doi:10.1046/j.1529-8817.2001.01052.x.
43. Shi D, Xu Y, Morel FMM, (2009) Effects of the pH/pCO2 control method on medium chemistry and phytoplankton growth. Biogeosciences 6: 1199-1207 doi:10.5194/bg-6-1199-2009.
44. McGinn PJ, Jones MJ, Macdonald AB, Campbell DA, (2005) Light is required for low-CO2-mediated induction of transcripts encoding components of the CO2-concentrating mechanism in the cyanobacterium Synechococcus elongatus: analysis by quantitative reverse transcription- polymerase chain reaction. Canadian Journal of Botany 83: 711-720 doi:10.1139/b05-055.
45. Lewis E, Wallace D (1998) CO2SYS, Program Developed for CO2 System Calculations. ORNL/CDIAC-105.
46. Peng T-H, Takahashi T, Broecker WS, Olafsson J, (1987) Seasonal variability of carbon dioxide, nutrients and oxygen in the northern North Atlantic surface water: observations and a model. Tellus B 39B: 439-458 doi:10.1111/j.1600-0889.1987.tb00205.x.
47. Mehrbach C, Culberson C, Hawley J, Pytkowicz R, (1973) Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnology and Oceanography 18: 897-907 Available: http://www.aslo.org/lo/toc/vol_18/issue_6/0897.pdf. Accessed 2013 Jan 8.
48. MacGillivary ML, Ehrman JM, (2011) A readily available SEM substrate for a random orientation of diatom frustules. Diatom Research 26: 321-323 doi:10.1080/0269249X.2011.639145.
49. Ehrman JM, Kaczmarska I (2012) Strategies for high-throughput microscopy in algal research. Current Advances in algal taxonomy and its applications: Phylogenetic, ecological and applied perspective. W. Szafer Institute of Botany, Polish Academy of Sciences, Kraków. pp. 253-262.
50. Campbell DA, Tyystjärvi E, (2012) Parameterization of photosystem II photoinactivation and repair. Biochimica et Biophysica Acta (BBA)- Bioenergetics 1817: 258-265 doi:10.1016/j.bbabio.2011.04.010.
51. Wu H, Cockshutt AM, McCarthy A, Campbell DA, (2011) Distinctive Photosystem II Photoinactivation and Protein Dynamics in Marine Diatoms. Plant Physiology 156: 2184-2195 doi:10.1104/pp.111.178772.
52. Barnett AB (2007) Fireworx. Available: http://sourceforge.net/projects/fireworx. Accessed 2012 Apr 24.
53. Van Kooten O, Snel J, (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research 25: 147-150.
54. Brown C, Mackinnon J, Cockshutt A, Villareal T, Campbell D, (2008) Flux capacities and acclimation costs in Trichodesmium from the Gulf of Mexico. Marine Biology 154: 413-422 doi:10.1007/s00227-008-0933-z.
55. Jeffrey S, Humphrey G, (1975) New spectrophotometric equations for determining chlorophylls a1, b1, c1 and c2 in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen 167: 191-194.
56. Heath RL, Packer L, (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics 125: 189-198 doi:10.1016/0003-9861(68)90654-1.
57. Janknegt PJ, Van De Poll WH, Visser RJW, Rijstenbil JW, Buma AGJ, (2008) Oxidative stress responses in the marine antarctic diatom Chaetoceros brevis (Bacillariophyceae) during Photoacclimation. Journal of Phycology 44: 957-966 doi:10.1111/j.1529-8817.2008.00553.x.
58. Platt T, Gallegos C, Harrison W, (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. Journal of Marine Research 38: 687-701.
59. Wu H, Roy S, Alami M, Green BR, Campbell DA, (2012) Photosystem II Photoinactivation, Repair, and Protection in Marine Centric Diatoms. Plant Physiology 160: 464-476 doi:10.1104/pp.112.203067.
60. Raven JA, (1991) Physiology of inorganic C acquisition and implications for resource use efficiency by marine phytoplankton: relation to increased CO2 and temperature. Plant, Cell & Environment 14: 779-794 doi:10.1111/j.1365-3040.1991.tb01442.x.
61. Hopkinson BM, Xu Y, Shi D, McGinn PJ, Morel FMM, (2010) The effect of CO2 on the photosynthetic physiology of phytoplankton in the Gulf of Alaska. Limnology and Oceanography 55: 2011-2024 doi:10.4319/lo.2010.55.5.2011.
62. Cullen JJ, Lewis MR, (1988) The kinetics of algal photoadaptation in the context of vertical mixing. Journal of Plankton Research 10: 1039-1063 doi:10.1093/plankt/10.5.1039.
63. Takahashi S, Milward SE, Yamori W, Evans JR, Hillier W, et al. (2010) The solar action spectrum of photosystem II damage. Plant Physiology 153: 988-993 doi:10.1104/pp.110.155747.
64. Janknegt PJ, De Graaff CM, Van De Poll WH, Visser RJW, Rijstenbil JW, et al. (2009) Short-term antioxidative responses of 15 microalgae exposed to excessive irradiance including ultraviolet radiation. European Journal of Phycology 44: 525-539 doi:10.1080/09670260902943273.
65. Waring J, Klenell M, Bechtold U, Underwood GJC, Baker NR, (2010) Light-Induced Responses of Oxygen Photoreduction, Reactive Oxygen Species Production and Scavenging in Two Diatom Species. Journal of Phycology 46: 1206-1217 doi:10.1111/j.1529-8817.2010.00919.x.
66. Litchman E, Neale P, Banaszak A, (2002) Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: Photoprotection and repair. Limnology and Oceanography 47: 86-94.
67. Ingalls AE, Whitehead K, Bridoux MC, (2010) Tinted windows: The presence of the UV absorbing compounds called mycosporine-like amino acids embedded in the frustules of marine diatoms. Geochimica et Cosmochimica Acta 74: 104-115 doi:10.1016/j.gca.2009.09.012.
68. Fuhrmann T, Landwehr S, El Rharbi-Kucki M, Sumper M, (2004) Diatoms as living photonic crystals. Applied Physics B: Lasers and Optics 78: 257-260 doi:10.1007/s00340-004-1419-4.
69. Milligan AJ, Morel FMM, (2002) A Proton Buffering Role for Silica in Diatoms. Science 297: 1848-1850 doi:10.1126/science.1074958.
70. Thomas S, Campbell DA, (2013) Photophysiology of Bolidomonas pacifica. Journal of Plankton Research In press.
71. Grouneva I, Gollan P, Kangasjärvi S, Suorsa M, Tikkanen M, et al. (2012) Phylogenetic viewpoints on regulation of light harvesting and electron transport in eukaryotic photosynthetic organisms. Planta pp. 1-14 doi:10.1007/s00425-012-1744-5.
72. Morel A, Bricaud A, (1981) Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep Sea Research Part A Oceanographic Research Papers 28: 1375-1393 doi:10.1016/0198-0149(81)90039-X.
73. Finkel Z, (2007) Light Absorption and Size Scaling of Light-Limited Metabolism in Marine Diatoms. pp. 1-10.
74. Huner NP, Öquist G, Sarhan F, (1998) Energy balance and acclimation to light and cold. Trends in Plant Science 3: 224-230 doi:10.1016/S1360-1385(98)01248-5.
75. Nixon P, Michoux F, Yu J, Boehm M, Komenda J, (2010) Recent advances in understanding the assembly and repair of photosystem II. Annals of Botany 106: 1-16 doi:10.1093/aob/mcq059.
76. Hong Y, Hu H-Y, Li F-M, (2008) Growth and physiological responses of freshwater green alga Selenastrum capricornutum to allelochemical ethyl 2-methyl acetoacetate (EMA) under different initial algal densities. Pesticide Biochemistry and Physiology 90: 203-212 doi:10.1016/j.pestbp.2007.11.009.
77. Burey SC, Poroyko V, Ergen ZN, Fathi-Nejad S, Schüller C, et al. (2007) Acclimation to low [CO2] by an inorganic carbon-concentrating mechanism in Cyanophora paradoxa. Plant, Cell & Environment 30: 1422-1435 doi:10.1111/j.1365-3040.2007.01715.x.
78. Nishiyama Y, Allakhverdiev S, Murata N, (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta 1757: 742-749 doi:10.1016/j.bbabio.2006.05.013.
79. Oguchi R, Terashima I, Kou J, Chow WS, (2011) Operation of dual mechanisms that both lead to photoinactivation of Photosystem II in leaves by visible light. Physiologia plantarum 142: 47-55 doi:10.1111/j.1399-3054.2011.01452.x.
80. Vass I, (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiologia Plantarum 142: 6-16 doi:10.1111/j.1399-3054.2011.01454.x.
81. Finkel ZV, Beardall J, Flynn KJ, Quigg A, Rees TAV, et al. (2010) Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research 32: 119-137 doi:10.1093/plankt/fbp098.
82. Chen B, Liu H, Landry MR, Chen M, Sun J, et al. (2009) Estuarine nutrient loading affects phytoplankton growth and microzooplankton grazing at two contrasting sites in Hong Kong coastal waters. Marine Ecology Progress Series 379: 77-90 doi:10.3354/meps07888.