Photophysiological responses of marine diatoms to elevated CO2 and decreased pH: A review

Functional Plant Biology

Volumn 41, Issue 5, 2014, Pages 449-459

  Gao, Kunshan ^a   Campbell, Douglas A ^b  

^a XIAMEN UNIVERSITY   (China)

^b MOUNT ALLISON UNIVERSITY   (Canada)

Author keywords

Bacillariophyceae; diatom; ocean acidification; photoinhibition; photosynthesis

Indexed keywords

ACIDIFICATION; CARBON DIOXIDE; CARBON SEQUESTRATION; DIATOM; GROWTH RATE; INHIBITION; LITERATURE REVIEW; MARINE ECOSYSTEM; MESOCOSM; PH; PHOTOSYNTHESIS; PHYSIOLOGICAL RESPONSE; PRIMARY PRODUCTION;

EID: 84897992629     PISSN: 14454408     EISSN: None     Source Type: Journal    
DOI: 10.1071/FP13247     Document Type: Article

References (128)

1. Allen AE, Dupont CL, Oborník M, Horák A, Nunes-Nesi A, McCrow JP, Zheng H, Johnson DA, Hu H, Fernie AR, Bowler C (2011) Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473, 203-207. doi:10.1038/nature10074
2. Aro E, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochimica et Biophysica Acta (BBA)-Bioenergetics 1143, 113-134. doi:10.1016/0005-2728 (93)90134-2
3. Barton AD, Finkel ZV, Ward BA, Johns DG, Follows MJ (2013) On the roles of cell size and trophic strategy in North Atlantic diatom and dinoflagellate communities. Limnology and Oceanography 58, 254-266. doi:10.4319/lo.2013.58.1. 0254
4. Bartual A, Galvez JA (2002) Growth and biochemical composition of the diatom Phaeodactylum tricornutum at different pH and inorganic carbon levels under saturating and subsaturating light regimes. Botanica Marina 45, 491-501. doi:10.1515/BOT.2002.052
5. Beardall J, Sobrino C, Stojkovic S (2009) Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers. Photochemical&photobiological sciences: Official journal of the European Photochemistry Association and the European Society for Photobiology 8, 1257-1265. doi:10.1039/b9pp00034h
6. Boelen P, Van de Poll WH, Van der Strate HJ, Neven IA, Beardall J, Buma AGJ (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
7. Bouma TJ, Visser R, Janssen JHJA, Kock MJ, Leeuwen PH, Lambers H (1994) Respiratory energy requirements and rate of protein turnover in vivo determined by the use of an inhibitor of protein synthesis and a probe to assess its effect. Physiologia Plantarum 92, 585-594. doi:10.1111/j.1399-3054.1994.tb03027. x
8. Brewer PG, Peltzer ET (2009) Limits to marine life. Science 324, 347-348. doi:10.1126/science.1170756
9. Burkhardt S, Riebesell U (1997) CO2 availability affects elemental composition (C :N: P) of the marine diatom Skeletonema costatum. Marine Ecology Progress Series 155, 67-76. doi:10.3354/meps155067
10. Burkhardt S, Zondervan I, Riebesell U (1999) Effect of CO2 concentration on the C:N: P ratio in marine phytoplankton: a species comparison. Limnology and Oceanography 44, 683-690. doi:10.4319/lo.1999.44.3. 0683
11. Burkhardt S, Amoroso G, Riebesell U (2001) CO2 and HCO3-uptake in marine diatoms acclimated to different CO2 concentrations. Limnology and Oceanography 46, 1378-1391. doi:10.4319/lo.2001.46.6.1378
12. Caldeira K, Wickett ME (2003) Oceanography: anthropogenic carbon and ocean pH. Nature 425, 365. doi:10.1038/425365a
13. CampbellDA,Hossain Z, CockshuttAM,Zhaxybayeva O,WuH, LiG(2013) Photosystem II protein clearance and FtsH function in the diatom Thalassiosira pseudonana. Photosynthesis Research 115, 43-54. doi:10.1007/s11120-013-9809-2
14. Chen X, Gao K (2003) Effect of CO2 concentrations on the activity of photosynthetic CO2 fixation and extracelluar carbonic anhydrase in the marine diatom Skeletonema costatum. Chinese Science Bulletin 48, 2616-2620. doi:10.1360/03wc0084
15. Chen X, Gao K (2004a) Photosynthetic utilisation of inorganic carbon and its regulation in the marine diatom Skeletonema costatum. Functional Plant Biology 31, 1027-1033. doi:10.1071/FP04076
16. Chen X, GaoK(2004b) Characterization of diurnal photosynthetic rhythms in the marine diatom Skeletonema costatum grown in synchronous culture under ambient and elevated CO2. Functional Plant Biology 31, 399-404. doi:10.1071/FP03240
17. Chen S, Gao K (2011) Solar ultraviolet radiation and CO2-induced ocean acidification interacts to influence the photosynthetic performance of the red tide alga Phaeocystis globosa (Prymnesiophyceae). Hydrobiologia 675, 105-117. doi:10.1007/s10750-011-0807-0
18. Collins S, Bell G (2004) Phenotypic consequences of 1000 generations of selection at elevated CO2 in a green alga. Nature 431, 566-569. doi:10.1038/nature02945
19. Collins S, Sültemeyer D, Bell G (2006) Changes in C uptake in populations of Chlamydomonas reinhardtii selected at high CO2. Plant, Cell & Environment 29, 1812-1819. doi:10.1111/j.1365-3040.2006.01559.x
20. 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
21. Doney SC (2006) Oceanography: plankton in a warmer world. Nature 444, 695-696. doi:10.1038/444695a
22. Edelman M, Mattoo AK (2008) D1-protein dynamics in photosystem II: the lingering enigma. Photosynthesis Research 98, 609-620. doi:10.1007/s11120-008- 9342-x
23. Elzenga JTM, Prins HBA, Stefels J (2000) The role of extracellular carbonic anhydrase activity in inorganic carbon utilization of Phaeocystis globosa (Pyrmnesiophyceae): a comparison with other marine algae using isotopic disequilibrium technique. Limnology and Oceanography 45, 372-380. doi:10.4319/lo.2000.45.2.0372
24. Engel A (2002) Direct relationship between CO2 uptake and transparent exopolymer particles production in natural phytoplankton. Journal of Plankton Research 24, 49-53. doi:10.1093/plankt/24.1.49
25. Falkowski PG, Oliver MJ (2007) Mix and match: how climate selects phytoplankton. Nature Reviews. Microbiology 5, 813-819. doi:10.1038/nrmicro1751
26. Feely RA, Sabine CL, Lee K, Berelson W, Kleypas J, Fabry VJ, Millero FJ (2004) Impact of anthropogenic CO2 on the CaCO3 system in the oceans. Science 305, 362-366. doi:10.1126/science.1097329
27. Feng Y, Hare CE, Leblanc K, Rose JM, Zhang Y, DiTullio GR, Lee P, Wilhelm S, Rowe JM, Sun J, Nemcek N, Gueguen C, Passow U, Benner I, Brown C, HutchinsDA(2009) Effects of increasedpCO2 and temperature on the North Atlantic spring bloom. I. The phytoplankton community and biogeochemical response. Marine Ecology Progress Series 388, 13-25. doi:10.3354/meps08133
28. Feng Y, Hare CE, Rose JM, Handy SM, DiTullio GR, Lee PA, SmithWOJr, Peloquin J, Tozzi S, Sun J, Zhang Y, Dunbar RB, Long MC, Sohst B, Lohan M, Hutchins DA (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
29. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-240. doi:10.1126/science.281.5374.237
30. Finkel ZV, Sebbo J, Feist-Burkhardt S, Irwin AJ, Katz ME, Schofield OME, Young JR, FalkowskiPG (2007)Auniversal driver of macroevolutionary change in the size of marine phytoplankton over the Cenozoic. Proceedings of the National Academy of Sciences of the United States of America 104, 20416-20420. doi:10.1073/pnas.0709381104
31. Finkel ZV, Beardall J, Flynn KJ, Quigg A, Rees TAV, Raven JA (2010) Phytoplankton in a changing world: cell size and elemental stoichiometry. Journal of Plankton Research 32, 119-137. doi:10.1093/plankt/fbp098
32. Flynn KJ, Blackford JC, BairdME,Raven JA, Clark DR,Beardall J, Brownlee C, Fabian H, Wheeler GL (2012) Changes in pH at the exterior surface of plankton with ocean acidification. Nature Climate Change 2, 510-513. doi:10.1038/nclimate1696
33. Gao K, Ruan Z, Villafañe VE, Gattuso J-P, Helbling EW (2009) Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi. Limnology and Oceanography 54, 1855-1862. doi:10.4319/lo.2009.54.6.1855
34. Gao K, Helbling EW, Häder DP, Hutchins DA (2012a) Ocean acidification and marine primary producers under the sun: a review of interactions between CO2, warming, and solar radiation. Marine Ecology Progress Series 470, 167-189. doi:10.3354/meps10043
35. Gao K, Xu J, Gao G, Li Y, Hutchins DA, Huang B, Wang L, Zheng Y, Jin P, Cai X, Häder D, Li W, Xu K, Liu N, Riebesell U (2012b) Rising CO2 and increased light exposure synergistically reduce marine primary productivity. Nature Climate Change 2, 519-523.
36. Gattuso J-P, Hansson L (2011) 'Ocean acidification.' (Oxford University Press: Oxford)
37. Gattuso J-P, GaoK, Lee K, Rost B, SchulzKG(2010) Approaches and tools to manipulate the carbonate chemistry. In 'Guide to best practices for ocean acidification research and data reporting'. (Eds U Riebesell, VJ Fabry, L Hansson, JP Gattuso) pp. 41-52. (Publications Office of the European Union: Luxembourg)
38. Giordano M, Beardall J, Raven JA (2005) CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56, 99-131. doi:10.1146/annurev.arplant.56. 032604.144052
39. Guan W, Gao K (2008) Light histories influence the impacts of solar ultraviolet radiation on photosynthesis and growth in a marine diatom, Skeletonema costatum. Journal of Photochemistry and Photobiology. B, Biology 91, 151-156. doi:10.1016/j.jphotobiol.2008.03.004
40. Häder D-P (2011) Does enhanced solar UV-B radiation affect marine primary producers in their natural habitats? Photochemistry and Photobiology 87, 263-266. doi:10.1111/j.1751-1097.2011.00888.x
41. Haimovich-Dayan M, Garfinkel N, Ewe D, Marcus Y, Gruber A, Wagner H, Kroth PG, Kaplan A (2013) The role of C4 metabolism in the marine diatom Phaeodactylum tricornutum. New Phytologist 197, 177-185. doi:10.1111/j.1469- 8137.2012.04375.x
42. Harada H, Nakajima K, Sakaue K, Matsuda Y (2006) CO2 sensing at ocean surface mediated by cAMP in a marine diatom. Plant Physiology 142, 1318-1328. doi:10.1104/pp.106.086561
43. Hare CE, Leblanc K, DiTullio GR, Kudela RM, Zhang Y, Lee PA, Riseman S, Hutchins DA (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
44. Hein M, Sand-Jensen K (1997) CO2 increases oceanic primary production. Nature 388, 526-527. doi:10.1038/41457
45. Hervé V, Derr J, Douady S, Quinet M, Moisan L, Lopez PJ (2012) Multiparametric analyses reveal the pH-dependence of silicon biomineralization in diatoms. PLoS ONE 7, e46722. doi:10.1371/journal.pone.0046722
46. Hinder SL, Hays GC, Edwards M, Roberts EC, Walne AW, Gravenor MB (2012) Changes in marine dinoflagellate and diatom abundance under climate change. Nature Climate Change 2, 271-275. doi:10.1038/nclimate1388
47. Hopkinson BM, Dupont CL, Allen AE, Morel FMM(2011) Efficiency of the CO2-concentrating mechanism of diatoms. Proceedings of the National Academy of Sciences of the United States of America 108, 3830-3837. doi:10.1073/pnas. 1018062108
48. Hopkinson BM, Meile C, Shen C (2013) Quantification of extracellular carbonic anhydrase activity in two marine diatoms and investigation of its role. Plant Physiology 162, 1142-1152. doi:10.1104/pp.113.217737
49. Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell K, Johnson CA (2001) 'IPCC climate change: the scientific basis.' (Cambridge University Press: Cambridge, UK)
50. Ihnken S, Roberts S, Beardall J (2011) Differential responses of growth and photosynthesis in the marine diatom Chaetoceros muelleri to CO2 and light availability. Phycologia 50, 182-193. doi:10.2216/10-11.1
51. Isensee K, Erez J, Stoll H (2013) Detection of a variable internal Ci pool in Thalassiosira weissflogii (Heterokontophyta) and Emiliania huxleyi (Haptophyta) in response to changes in the seawater carbon system. Physiologia Plantarum doi:10.1111/ppl.12096n press
52. Jin P, Gao K, Villafañe VE, Campbell DA, Helbling W (2013a) Ocean acidification alters the photosynthetic responses of a coccolithophorid to fluctuating UV and visible radiation. Plant Physiology 162, 2084-2094. doi:10.1104/pp.113.219543
53. Jin P, Gao K, Beardall J (2013b) Evolutionary responses of a coccolithophorid Gephyrocapsa oceanica to ocean acidification. Evolution 67, 1869-1878. doi:10.1111/evo.12112
54. Johnson VR, Brownlee C, Rickaby REM, Graziano M, Milazzo M, Hall-Spencer JM (2013) Responses of marine benthic microalgae to elevated CO2. Marine Biology 160, 1813-1824. doi:10.1007/s00227-011-1840-2
55. Kaplan A, Badger MR, Berry JA (1980) Photosynthesis and the intracellular inorganic carbon pool in the bluegreen alga Anabaena variabilis: response to external CO2 concentration. Planta 149, 219-226. doi:10.1007/BF00384557
56. KeyT, Mccarthy A, Campbell D, Six C,RoyS, FinkelZ(2010) Cell size tradeoffs govern light exploitation strategies in marine phytoplankton. Environmental Microbiology 12, 95-104. doi:10.1111/j.1462-2920. 2009.02046.x
57. Kim J-M, Lee K, Shin K, Kang J-H, Lee H-W, Kim M, Jang P-G, Jang M-C (2006) The effect of seawater CO2 concentration on growth of a natural phytoplankton assemblage in a controlled mesocosm experiment. Limnology and Oceanography 51, 1629-1636. doi:10.4319/lo.2006. 51.4.1629
58. King AL, Sañudo-Wilhelmy SA, Leblanc K, Hutchins DA, Fu F (2011) CO2 and vitaminB12 interactions determine bioactive trace metal requirements of a subarctic Pacific diatom. ISME Journal 5, 1388-1396. doi:10.1038/ismej.2010. 211
59. KokB(1956)Onthe inhibition of photosynthesis by intense light. Biochimica et Biophysica Acta 21, 234-244. doi:10.1016/0006-3002(56)90003-8
60. Korb RE, Saville PJ, Johnston AM, Raven JA (1997) Sources of inorganic carbon for photosynthesis by three species of marine diatom. Journal of Phycology 33, 433-440. doi:10.1111/j.0022-3646.1997.00433.x
61. Lavaud J, Rousseau B, Etienne A-L (2004) General features of photoprotection by energy dissipation in planktonic diatoms (Bacillariophyceae). Journal of Phycology 40, 130-137. doi:10.1046/j.1529-8817.2004.03026.x
62. 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
63. Li G, CampbellDA(2013) RisingCO2 interacts with growth light and growth rate to alter photosystem II photoinactivation of the coastal diatom Thalassiosira pseudonana. PLoS ONE 8, e55562. doi:10.1371/journal. pone.0055562
64. Li Q, Canvin DT (1998) Energy sources for HCO3-and CO2 transport in air-grown cells of Synechococcus UTEX 625. Plant Physiology 116, 1125-1132. doi:10.1104/pp.116.3.1125
65. Li YH, Gao K, Villafañe VE, Helbling EW (2012a) Ocean acidification mediates photosynthetic response to UV radiation and temperature increase in the diatom Phaeodactylum tricornutum. Biogeosciences 9, 3931-3942. doi:10.5194/bg-9-3931-2012
66. Li W, Gao K, Beardall J (2012b) Interactive effects of ocean acidification and nitrogen-limitation on the diatom Phaeodactylum tricornutum. PLoS ONE 7, e51590. doi:10.1371/journal.pone.0051590
67. Lohbeck KT, Riebesell U, Reusch TBH (2012) Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geoscience 5, 346-351. doi:10.1038/ngeo1441
68. 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
69. Matsuda Y, Hara T, Colman B (2001) Regulation of the induction of bicarbonate uptake by dissolved CO2 in the marine diatom, Phaeodactylum tricornutum. Plant, Cell & Environment 24, 611-620. doi:10.1046/j.1365-3040. 2001.00702.x
70. McCarthy A, Rogers SP, Duffy SJ, Campbell DA (2012) Elevated carbon dioxide differentially alters the photophysiology of Thalassiosira pseudonana (Bacillariophyceae) and Emiliania huxleyi (Haptophyta). Journal of Phycology 48, 635-646. doi:10.1111/j.1529-8817.2012.01171.x
71. MejíaLM,Isensee K, Méndez-Vicente A, Pisonero J, Shimizu N, GonzálezC, Monteleone B, Stoll H (2013) B content and Si/C ratios from cultured diatoms (Thalassiosira pseudonana and Thalassiosira weissflogii): relationship to seawater pH and diatom carbon acquisition. Geochimica et Cosmochimica Acta 123, 322-337. doi:10.1016/j.gca. 2013.06.011
72. Millero FJ, Woosley R, Ditrolio B, Waters J (2009) Effect of ocean acidification on the speciation of metals in seawater. Oceanography 22, 72-85. doi:10.5670/oceanog.2009.98
73. Milligan AJ, MorelFMM(2002)Aproton buffering role for silica in diatoms. Science 297, 1848-1850. doi:10.1126/science.1074958
74. Mitchell JG, Seuront L, Doubell MJ, Losic D, Voelcker NH, Seymour J, LalR (2013) The role of diatom nanostructures in biasing diffusion to improve uptake in a patchy nutrient environment. PLoS ONE 8, e59548. doi:10.1371/journal.pone. 0059548
75. Morel FMM, Reinfelder JR, Roberts SB, Chamberlain CP, Lee JG, Yee D (1994) Zinc and carbon co-limitation of marine phytoplankton. Nature 369, 740-742. doi:10.1038/369740a0
76. Mutshinda CM, Troccoli-Ghinaglia L, Finkel ZV, Müller-Karger FE, Irwin AJ (2013) Environmental control of the dominant phytoplankton in the Cariaco basin: a hierarchical Bayesian approach. Marine Biology Research 9, 246-260. doi:10.1080/17451000.2012.731693
77. Nagao R, Tomo T, Noguchi E, Suzuki T, Okumura A, Narikawa R, Enami I, Ikeuchi M (2012) Proteases are associated with a minor fucoxanthin chlorophyll a/c-binding protein from the diatom, Chaetoceros gracilis. Biochimica et Biophysica Acta 1817, 2110-2117. doi:10.1016/j.bbabio. 2012.08.005
78. Nakajima K, Tanaka A, Matsuda Y (2013) SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proceedings of the National Academy of Sciences of the United States of America 110, 1767-1772. doi:10.1073/pnas.1216234110
79. Nimer NA, Iglesias-Rodriguez MD, Merrett MJ (1997) Bicarbonate utilization by marine phytoplankton species. Journal of Phycology 33, 625-631. doi:10.1111/j.0022-3646.1997.00625.x
80. Nixon PJ, 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
81. Niyogi KK, Li X-P, Rosenberg V, Jung H-S (2005) Is PsbS the site of nonphotochemical quenching in photosynthesis? Journal of Experimental Botany 56, 375-382. doi:10.1093/jxb/eri056
82. Orellana M, Ashworth J, Lee A, Armbrust EV (2013) 'A systems approach to diatom responses to ocean acidification.' (The Molecular Life of Diatoms EMBO Workshop: Paris)
83. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, GnanadesikanA, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, MouchetA, NajjarRG,Plattner G, RodgersKB,Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig M, Yamanaka Y, YoolA(2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437, 681-686. doi:10.1038/nature04095
84. Pörtner HO, Farrell AP (2008) Physiology and climate change. Science 322, 690-692. doi:10.1126/science.1163156
85. 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
86. Raven JA (1993) Limits on growth rates. Nature 361, 209-210. doi:10.1038/361209a0
87. Raven JA (2010) Inorganic carbon acquisition by eukaryotic algae: four current questions. 106, 123-134.
88. Raven JA, JohnstonAM(1991) Mechanisms of inorganic-carbon acquisition in marine phytoplankton and their implications for the use of other resources. Limnology and Oceanography 36, 1701-1714. doi:10.4319/lo.1991.36.8.1701
89. Raven JA, Giordano M, Beardall J, Maberly SC (2011) Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynthesis Research 109, 281-296. doi:10.1007/s11120-011-9632-6
90. Reinfelder JR (2011) Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annual Review of Marine Science 3, 291-315. doi:10.1146/annurev- marine-120709-142720
91. Reinfelder JR, Kraepiel AM, MorelFM(2000) UnicellularC4 photosynthesis in a marine diatom. Nature 407, 996-999. doi:10.1038/35039612
92. Reinfelder JR, Milligan AJ, MorelFMM(2004) The role of theC4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiology 135, 2106-2111. doi:10.1104/pp.104.041319
93. Riebesell U, Tortell PD (2011) Effects of ocean acidification on pelagic organisms and ecosystems. In 'Ocean acidification'. (Oxford University Press: Oxford)
94. Riebesell U, Wolf-Gladrow DA, Smetacek V (1993) Carbon dioxide limitation of marine phytoplankton growth rates. Nature 361, 249-251. doi:10.1038/361249a0
95. Roberts K, Granum E, Leegood RC, Raven JA (2007a)C3 andC4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiology 145, 230-235. doi:10.1104/pp.107.102616
96. Roberts K, Granum E, Leegood RC, Raven JA (2007b) Carbon acquisition by diatoms. Photosynthesis Research 93, 79-88. doi:10.1007/s11120-007-9172-2
97. Rost B, Riebesell U, Burkhardt S, Sültemeyer D (2003) Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography 48, 55-67. doi:10.4319/lo.2003.48.1.0055
98. Sabine CL, Feely RA, Gruber N, KeyRM,Lee K, Bullister JL, WanninkhofR, Wong CS, Wallace DWR, Tilbrook B, Millero FJ, Peng T, Kozyr A, Ono T, Rios AF (2004) The oceanic sink for anthropogenic CO2. Science 305, 367-371. doi:10.1126/science.1097403
99. 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
100. Shatwell T, Nicklisch A, Köhler J (2012) Temperature and photoperiod effects on phytoplankton growing under simulated mixed layer light fluctuations. Limnology and Oceanography 57, 541-553. doi:10.4319/lo.2012.57.2. 0541
101. Sims PA, Mann DG, Medlin LK (2006) Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45, 361-402. doi:10.2216/05-22.1
102. Six C, Finkel ZV, Irwin AJ, CampbellDA(2007) Light variability illuminates niche-partitioning among marine picocyanobacteria. PLoSONE2, e1341. doi:10.1371/journal.pone.0001341
103. Six C, Sherrard R, Lionard M, Roy S, Campbell D(2009) Photosystem II and pigment dynamics among ecotypes of the green alga Ostreococcus. Plant Physiology 151, 379-390. doi:10.1104/pp.109.140566
104. Sobrino C, WardML,Neale PJ (2008) Acclimation to elevated carbon dioxide and ultraviolet radiation in the diatom Thalassiosira pseudonana: effects on growth, photosynthesis, and spectral sensitivity of photoinhibition. Limnology and Oceanography 53, 494-505. doi:10.4319/lo.2008. 53.2.0494
105. Steinacher M, Joos F, Frölicher TL, Bopp L, Cadule P, Cocco V, Doney SC, Gehlen M, Lindsay K, Moore JK, Schneider B, Segschneider J (2010) Projected 21st century decrease in marine productivity: a multi-model analysis. Biogeosciences 7, 979-1005. doi:10.5194/bg-7-979-2010
106. Sugie K, Yoshimura T (2013) Effects of pCO2 and iron on the elemental composition and cell geometry of the marine diatom Pseudo-nitzschia pseudodelicatissima (Bacillariophyceae). Journal of Phycology 49, 475-488. doi:10.1111/jpy.12054
107. Sukenik A, Tchernov D, Kaplan A, Huertas E, Lubian LM, Livne A (1997) Uptake, efflux, and photosynthetic utilization of inorganic carbon by the marine eustigmatophyte Nannochloropsis Sp.1. Journal of Phycology 33, 969-974. doi:10.1111/j.0022-3646.1997.00969.x
108. Sültemeyer D, Schmidt C, Fock HP (1993) Carbonic anhydrases in higher plants and aquatic microorganisms. Physiologia Plantarum 88, 179-190. doi:10.1111/j.1399-3054.1993.tb01776.x
109. Sun J, Hutchins DA, Feng Y, Seubert EL, Caron DA, Fu F-X (2011) Effects of changing pCO2 and phosphate availability on domoic acid production and physiology of the marine harmful bloom diatom Pseudo-nitzschia multiseries. Limnology and Oceanography 56, 829-840. doi:10.4319/lo.2011.56.3.0829
110. Tatters AO, Fu F-X, Hutchins DA (2012) High CO2 and silicate limitation synergistically increase the toxicity of Pseudo-nitzschia fraudulenta. PLoS ONE 7, e32116. doi:10.1371/journal.pone.0032116
111. Tchernov D, Hassidim M, Luz B, Sukenik A, Reinhold L, Kaplan A (1997) Sustained net CO2 evolution during photosynthesis by marine microorganisms. Current biology: CB 7 723-728. doi:10.1016/S0960-9822(06)00330-7
112. Torstensson A, Chierici M, Wulff A (2012) The influence of increased temperature and carbon dioxide levels on the benthic/sea ice diatom Navicula directa. Polar Biology 35, 205-214. doi:10.1007/s00300-011-1056-4
113. Tortell PD, Rau GH, Morel FMM (2000) Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnology and Oceanography 45, 1485-1500. doi:10.4319/lo.2000.45.7.1485
114. Tortell PD, Payne CD, Li YY, Trimborn S, Rost B, SmithWO, Riesselman C, Dunbar RB, Sedwick P, DiTullio GR (2008) CO2 sensitivity of Southern Ocean phytoplankton. Geophysical Research Letters 35, L04605. doi:10.1029/2007GL032583
115. Trimborn S, Wolf-Gladrow D, Richter K-U, Rost B (2009) The effect of pCO2 on carbon acquisition and intracellular assimilation in four marine diatoms. Journal of Experimental Marine Biology and Ecology 376, 26-36. doi:10.1016/j.jembe.2009.05.017
116. Tsuzuki M, Miyachi S (1989) The function of carbonic anhydrase in aquatic photosynthesis. Aquatic Botany 34, 85-104. doi:10.1016/0304-3770(89) 90051-X
117. Veron JEN (2008) Mass extinctions and ocean acidification: biological constraints on geological dilemmas. Coral Reefs 27, 459-472. doi:10.1007/s00338-008-0381-8
118. Waring J, Klenell M, Bechtold U, Underwood GJC, Baker NR (2010) Lightinduced 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
119. Wingler A, Lea PJ, Quick WP, Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 355, 1517-1529. doi:10.1098/rstb.2000.0712
120. Woodger FJ, Badger MR, Price GD (2005) Sensing of inorganic carbon limitation in Synechococcus PCC7942 is correlated with the size of the internal inorganic carbon pool and involves oxygen. Plant Physiology 139, 1959-1969. doi:10.1104/pp.105.069146
121. WuY, Gao K, RiebesellU (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
122. 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
123. Wu X, Gao G, Giordano M, Gao K (2012a) Growth and photosynthesis of a diatom grown under elevated CO2; in the presence of solar UV radiation. Fundamental and Applied Limnology. Archiv fuer Hydrobiologie 180, 279-290.
124. Wu H, Roy S, Alami M, Green BR, Campbell DA (2012b) Photosystem II photoinactivation, repair, and protection in marine centric diatoms. Plant Physiology 160, 464-476. doi:10.1104/pp.112.203067
125. Xu JT, Gao K (2012) Future CO2-induced ocean acidification mediates physiological performance of a green tide alga. Plant Physiology 160, 1762-1769. doi:10.1104/pp.112.206961
126. 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
127. Zhu S-H, Green BR (2010) Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochimica et Biophysica Acta 1797, 1449-1457. doi:10.1016/j.bbabio. 2010.04.003
128. Zou D, Gao K, Luo H (2011) Short-and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (sargassaceae, Phaeophyta) grown at low and high N supplies. Journal of Phycology 47, 87-97. doi:10.1111/j.1529-8817. 2010.00929.x