Evolutionary potential of marine phytoplankton under ocean acidification

Evolutionary Applications

Volumn 7, Issue 1, 2014, Pages 140-155

  Collins, Sinéad ^a   Rost, Björn ^b   Rynearson, Tatiana A ^c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^c UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

Adaptation; Experimental evolution; Global change; Ocean acidification; Phytoplankton

Indexed keywords

EID: 84891951189     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12120     Document Type: Article

References (119)

1. Alpermann, T. J., U. Tillmann, B. Beszteri, A. D. Cembella, and U. John 2010. Phenotypic and genotypic diversity in a planktonic population of the toxigenic marine dinoflagellate Alexandrium tamarense (Dinophyceae). Journal of Phycology 46:18-32.
2. Aparicio, S., J. Chapman, E. Stupka, N. Putnam, J.-M. Chia, P. Dehal, A. Christoffels et al. 2002. Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297:1301-1310.
3. Armbrust, E. V., J. A. Berges, C. Bowler, B. R. Green, D. Martinez, N. H. Putnam, S. G. Zhou et al. 2004. The genome of the diatomThalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79-86.
4. 2 in the Southern Ocean. Science 283:365-367.
5. Bach, L. T., U. Riebesell, S. Sett, S. Febiri, P. Rzepka, and K. G. Schulz 2012. An approach for particle sinking velocity measurements in the 3-400 μm size range and considerations on the effect of temperature on sinking rates. Marine Biology 159:1853-1864.
6. 2-concentrating mechanisms in algae. Canadian Journal of Botany 76:1052-1071.
7. Balch, W. M., K. A. Kilpatric, and C. C. Trees 1996. The 1991 coccolithophore bloom in the central North Atlantic. 1. Optical properties and factors affecting their distribution. Limnology and Oceanography 41:1669-1683.
8. Beaufort, L., I. Probert, T. de Garidel-Thoron, E. M. Bendif, D. Ruiz-Pino, N. Metzl, C. Goyet et al. 2011. Sensitivity of coccolithophores to carbonate chemistry and ocean acidification. Nature 476:80-83.
9. Becks, L., S. P. Ellner, L. E. Jones, and N. G. J. Hairston 2010. Reduction of adaptive genetic diversity radically alters eco-evolutionary community dynamics. Ecology Letters 13:989-997.
10. 2. Philosophical Transactions of the Royal Society B: Biological Sciences 368:1627 20130049.
11. Bonduriansky, R., A. J. Crean, and T. Day 2012. The implications of nongenetic inheritance for evolution in changing environments. Evolutionary Applications 5:192-201.
12. Boyd, P. W., T. A. Rynearson, E. A. Armstrong, F. Fu, K. Hayashi, Z. Hu, D. A. Hutchins et al. 2013. Marine phytoplankton temperature versus growth responses from polar to tropical waters - outcome of a scientific community-wide study. PLoS ONE 8:e63091.
13. Brand, L. E. 1981. Genetic variability in reproduction rates in marine phytoplankton populations. Evolutionary Biology 35:1117-1127.
14. Brand, L. E. 1990. Review of genetic variation in marine phytoplankton species and the ecological implications. Biological Oceanography 6:397-409.
15. Bratbak, G., M. Heldal, S. Norland, and T. F. Thingstad 1990. Viruses as partners in spring bloom microbial trophodynamics. Applied and Environmental Microbiology 56:1400-1405.
16. 2 concentration on C:N:P ratio in marine phytoplankton: a species comparison. Limnology and Oceanography 44:683-690.
17. Caldeira, K., and M. E. Wickett 2003. Oceanography: anthropogenic carbon and ocean pH. Nature 425:365-365.
18. Caron, D. A., and D. A. Hutchins 2013. The effects of changing climate on microzooplankton grazing and community structure: drivers, predictions and knowledge gaps. Journal of Plankton Research 35:235-252.
19. Carpenter, E. J., and R. R. L. Guillard 1971. Intraspecific differences in nitrate half-saturation constants for three species of marine phytoplankton. Ecology 52:183-185.
20. Casteleyn, G., K. Evans, T. Backeljau, S. D'hondt, V. Chepurnov, K. Sabbe, and W. Vyverman 2009. Lack of population genetic structuring in the marine planktonic diatom Pseudo-nitzschia pungens (Bacillariophyceae) in a heterogeneous area in the Southern Bight of the North Sea. Marine Biology 156:1149-1158.
21. Casteleyn, G., F. Leliaert, T. Backeljau, A.-E. Debeer, Y. Kotaki, L. Rhodes, N. Lundholm et al. 2010. Limits to gene flow in a cosmopolitan marine planktonic diatom. Proceedings of the National Academy of Sciences 107:12952-12957.
22. Chevin, L. M., R. Lande, and G. M. Mace 2010. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS biology 8:e1000357.
23. Cho, S. Y., S. Nagai, G. Nishitani, and M. S. Han 2009. Development of compound microsatellite markers in red-tide-causing dinoflagellate Akashiwo sanguinea (Dinophyceae). Molecular Ecology Resources 9:915-917.
24. 2. Proceedings of the Royal Society B: Biological Sciences 278:247-255.
25. Collins, S. 2011b. Many possible worlds: expanding the ecological scenarios in experimental evolution. Evolutionary Biology 38:3-14.
26. 2 in a green alga. Nature 431:566-569.
27. Conover, D. O., and E. T. Schultz 1995. Phenotypic similarity and the evolutionary significance of countergradient variation. Trends in Ecology & Evolution 10:248-252.
28. Cooper, T., and R. Lenski 2010. Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evolutionary Biology 10:11.
29. Crawford, R. M. 1995. The role of sex in the sedimentation of a marine diatom bloom. Limnology and Oceanography 40:200-204.
30. 2 and decreased pH. PLoS ONE 6:e26695.
31. von Dassow, P., and M. Montresor 2011. Unveiling the mysteries of phytoplankton life cycles: patterns and opportunities behind complexity. Journal of Plankton Research 33:3-12.
32. De La Rocha, C. L., and U. Passow 2007. Factors influencing the sinking of POC and the efficiency of the biological carbon pump. Deep Sea Research Pt II 54:639-658.
33. Dehal, P., Y. Satou, R. K. Campbell, J. Chapman, B. Degnan, A. De Tomaso, B. Davidson et al. 2002. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298:2157-2167.
34. DeLong, E. F. 2009. The microbial ocean from genomes to biomes. Nature 459:200-206.
35. 2 problem. Annual Review of Marine Science 1:169-192.
36. Doyle, R. W. 1975. Upwelling, clone selection, and the characteristic shape of nutrient uptake curves. Limnology and Oceanography 20:487-489.
37. Draghi, J. A., and M. C. Whitlock 2012. Phenotypic plasticity facilitates mutational variance, genetic variance, and evolvability along the major axis of environmental variation. Evolutionary Biology 66:2891-2902.
38. Egleston, E. S., C. L. Sabine, and F. M. M. Morel 2010. Revelle revisited: buffer factors that quantify the response of ocean chemistry to changes in DIC and alkalinity. Global Biogeochemical Cycles 24:GB1002.
39. Elena, S. F., and R. E. Lenski 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nature Reviews Genetics 4:457-469.
40. Ellstrand, N. C., and M. L. Roose 1987. Patterns of genotypic diversity in clonal plant species. American Journal of Botany 74:123-131.
41. Erdner, D. L., M. Richlen, L. A. R. McCauley, and D. M. Anderson 2011. Diversity and dynamics of a widespread bloom of the toxic dinoflagellate Alexandrium fundyense. PLoS ONE 6:e22965.
42. Evans, K. M., S. S. Bates, L. K. Medlin, and P. K. Hayes 2004. Microsatellite marker development and genetic variation in the toxic marine diatom Pseudo-nitzschia multiseries (Bacillariophyceae). Journal of Phycology 40:911-920.
43. Evans, K. M., S. F. Kuhn, and P. K. Hayes 2005. High levels of genetic diversity and low levels of genetic differentiation in North Sea Pseudo-nitzschia pungens (Bacillariophyceae) populations. Journal of Phycology 41:506-514.
44. Falkowski, P., and J. A. Raven 2007. Aquatic Photosynthesis. Princeton University Press, Princeton, NJ.
45. Falkowski, P. G., R. T. Barber, and V. Smetacek 1998. Biogeochemical controls and feedbacks on ocean primary production. Science 281:200-206.
46. 2 world. Oceanography 22:36-47.
47. Field, C. B., M. J. Behrenfeld, J. T. Randerson, and P. Falkowski 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237-240.
48. Flynn, K. J., J. C. Blackford, M. E. Baird, J. A. Raven, D. R. Clark, J. Beardall, C. Brownlee et al. 2012. Changes in pH at the exterior surface of plankton with ocean acidification. Nature Climate Change 2:510-513.
49. Frada, M., I. Probert, M. J. Allen, W. H. Wilson, and C. de Vargas 2008. The 'Cheshire Cat' escape strategy of the coccolithophore Emiliania huxleyi in response to viral infection. Proceedings of the National Academy of Sciences 105:15944-15949.
50. 2 and phosphate availability control the toxicity of the harmful bloom dinoflagellate Karlodinium veneficum. Aquatic Microbiology and Ecology 59:55-65.
51. Fuhrman, J. A. 2009. Microbial community structure and its functional implications. Nature 459:193-199.
52. Gallagher, J. C. 1980. Population genetics of Skeletonema costatum (Bacillariophyceae) in Narragansett Bay. Journal of Phycology 16:464-474.
53. Gallagher, J. C. 1982. Physiological variation and electrophoretic banding patterns of genetically different seasonal popluations of Skeletonema costatum (Bacillariophyceae). Journal of Phycology 18:148-162.
54. Gerrish, P., and R. Lenski 1998. The fate of competing beneficial mutations in an asexual population. Genetica 102-103:127-144.
55. Ghalambor, C. K., J. K. McKay, S. P. Carroll, and D. N. Reznick 2007. Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Functional Ecology 21:394-407.
56. Godhe, A., and K. Härnström 2010. Linking the planktonic and benthic habitat: genetic structure of the marine diatom Skeletonema marinoi. Molecular Ecology 19:4478-4490.
57. Grimsley, N., B. Péquin, C. Bachy, H. Moreau, and G. Piganeau 2010. Cryptic sex in the smallest eukaryotic marine green alga. Molecular Biology and Evolution 27:47-54.
58. Härnström, K., M. Ellegaard, T. R. J. Andersen, and A. Godhe 2011. Hundred years of genetic structure in a sediment revived diatom population. Proceedings of the National Academy of Sciences 108:4252-4257.
59. Hayden, E. J., E. Ferrada, and A. Wagner 2011. Cryptic genetic variation promotes rapid evolutionary adaptation in an RNA enzyme. Nature 474:92-95.
60. Hofmann, M., and H.-J. Schellnhuber 2009. Oceanic acidification affects marine carbon pump and triggers extended marine oxygen holes. Proceedings of the National Academy of Sciences 106:3017-3022.
61. Holligan, P. M., E. Fernandez, J. Aiken, W. M. Balch, P. Boyd, P. H. Burkill, M. Finch et al. 1993. A biogeochemical study of the coccolithophore Emiliania huxleyi, in the North Atlantic. Global Biogeochemical Cycles 7:879-900.
62. Holtermann, K. E., S. S. Bates, V. L. Trainer, A. Odell, and V. E. Armbrust 2010. Mass sexual reproduction in the toxigenic diatoms Pseudo-nitzschia australis and P. pungens (Bacillariophyceae) on the Washington coast, USA. Journal of Phycology 46:41-52.
63. Hoppe, C. J. M., G. Langer, and B. Rost 2011. Emiliania huxleyi shows identical responses to elevated pCO2 in TA and DIC manipulations. Journal of Experimental Marine Biology and Ecology 406:54-62.
64. Hoppe, C. J. M., C. S. Hassler, C. D. Payne, P. D. Tortell, B. Rost, and S. Trimborn 2013. Iron limitation modulates ocean acidification effects on Southern Ocean phytoplankton communities. PLoS ONE 8:e79890.
65. Iglesias-Rodriguez, D., O. M. Schofield, J. Batley, L. K. Medlin, and P. K. Hayes 2006. Intraspecific genetic diversity in the marine cocolithophore Emiliania huxleyi (Prymnesiophyceae): the use of microsatellite analysis in marine phytoplankton population studies. Journal of Phycology 42:526-536.
66. Jewson, D. H. 1992. Size reduction, reproductive strategy and the life cycle of a centric diatom. Philosophical Transactions of the Royal Society B: Biological Sciences 335:191-213.
67. Jin, P., K. Gao, and J. Beardall 2013. Evolutionary responses of a coccolithophorid Geophyrocapsa oceanica to ocean acidification. Evolutionary Biology 67:1869-1878.
68. Klaas, C., and D. E. Archer 2002. Association of sinking organic matter with various types of mineral ballast in the deep sea: implications for the rain ratio. Global Biogeochemical Cycles 16:1116.
69. Koester, J. A., W. J. Swanson, and E. V. Armbrust 2013. Positive selection within a diatom species acts on putative protein interactions and transcriptional regulation. Molecular Biology and Evolution 30:422-434.
70. Kranz, S. A., D. Sültemeyer, K.-U. Richter, and B. Rost 2009. Carbon acquisition by Trichodesmium: the effect of pCO2 and diurnal changes. Limnology and Oceanography 54:548-559.
71. 2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: physiological responses. Plant physiology 154:334-345.
72. Kremp, A., A. Godhe, J. Egardt, S. Dupont, S. Suikkanen, S. Casabianca, and A. Penna 2012. Intraspecific variability in the response of bloom-forming marine microalgae to changed climate conditions. Ecology and Evolution 2:1195-1207.
73. Lande, R. 2009. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. Journal of Evolutionary Biology 22:1435-1446.
74. Langer, G., G. Nehrke, I. Probert, and P. Ziveri 2009. Strain-specific responses of Emiliania huxleyi to changing seawater carbonate chemistry. Biogeosciences 6:2637-2646.
75. Lohbeck, K. T., U. Riebesell, and T. B. H. Reusch 2012a. Adaptive evolution of a key phytoplankton species to ocean acidification. Nature Geoscience 5:917-917.
76. 2 adapted Emiliania huxleyi populations. Evolutionary Biology 67:1892-1900.
77. 2 on growth and competition in experimental phytoplankton communities. Global Change Biology 17:2525-2535.
78. 2 fails to evoke specific adaptation in seven freshwater phytoplankton species. Proceedings of the Royal Society B: Biological Sciences 280:20122598.
79. Lowe, C. D., D. J. S. Montagnes, L. E. Martin, and P. C. Watts 2010. High genetic diversity and fine-scale spatial structure in the marine flagellate Oxyrrhis marina (Dinophyceae) uncovered by microsatellite loci. PLoS ONE 5:e15557.
80. MacIntyre, H. L., T. M. Kana, and R. J. Geider 2000. The effect of water motion on short-term rates of photosynthesis by marine phytoplankton. Trends in Plant Science 5:12-17.
81. 2: interaction between ocean circulation and biology. Climate Dynamics 12:711-721.
82. Mann, D. G. 1988. Why didn't Lund see sex in Asterionella? A discussion of the diatom life cycle in nature. In F. E. Round, ed. Algae and the Aquatic Environment, pp. 384-412. Biopress, Bristol, UK.
83. McCauley, L. A., D. L. Erdner, S. Nagai, M. L. Richlen, and D. M. Anderson 2009. Biogeographic analysis of the globally distributed harmful algal bloom species Alexandrium minutum (Dinophyceae) based on rRNA gene sequences and microsatellite markers1. Journal of Phycology, 45:454-463.
84. Meehl, G. A., T. F. Stocker, W. D. Collins, P. Friedlingstein, A. T. Gaye, J. M. Gregory, A. Kitoh et al. 2007. IPCC. In S. Solomon, D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor, and H. L. Miller, eds. Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, pp. 747-846. Cambridge University Press, Cambridge, UK and New York, NY
85. Miklasz, K. A., and M. W. Denny 2010. Diatom sinkings speeds: improved predictions and insight from a modified Stokes'' law. Limnology and Oceanography 55:2513-2525.
86. Nagai, S., C. Lian, S. Yamaguchi, M. Hamaguchi, Y. Matsuyama, S. Itakura, H. Shimada et al. 2007. Microsatellite markers reveal population genetic structure of the toxic dinoflagellate Alexandrium tamarense (Dinophyceae) in Japanese coastal waters. Journal of Phycology 43:43-54.
87. Nagai, S., G. Nishitani, S. Sakamoto, T. Sugaya, C. K. Lee, C. H. Kim, S. Itakura et al. 2009. Genetic structuring and transfer of marine dinoflagellate Cochlodinium polykrikoides in Japanese and Korean coastal waters revealed by microsatellites. Molecular Ecology 18:2337-2352.
88. Nagai, S., S. Yamaguchi, C. L. Lian, Y. Matsuyama and S. Itakura 2006. Development of microsatellite markers in the noxious red tide-causing algae Heterosigma akashiwo (Raphidophyceae). Molecular Ecology Notes 6:477-479.
89. Nejstgaard, J. C., I. Gismervik, and P. T. Solberg 1997. Feeding and reproduction by Calanus finmarchicus, and microzooplankton grazing during mesocosm blooms of diatoms and the coccolithophore Emiliania huxleyi. Marine Ecology Progress Series 147:197-217.
90. Reinfelder, J. R. 2011. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annual Review of Marine Science 3:291-315.
91. Reinfelder, J. R. 2012. Carbon dioxide regulation of nitrogen and phosphorus in four species of marine phytoplankton. Marine Ecology Progress Series 466:57-67.
92. Richlen, M. L., D. L. Erdner, L. A. R. McCauley, K. Libera, and D. M. Anderson 2012. Extensive genetic diversity and rapid population differentiation during blooms of Alexandrium fundyense (Dinophyceae) in an isolated salt pond on Cape Cod, MA, USA. Ecology and Evolution 2:2583-2594.
93. 2. Nature 407:364-367.
94. 2 ocean. Nature 450:545-548.
95. Rohwer, F., D. Prangishvili, and D. Lindell 2009. Roles of viruses in the environment. Environmental Microbiology 11:2771-2774.
96. 2 and their modulation by light in the life-cycle stages of the coccolithophore Emiliania huxleyi. Limnology and Oceanography 57:607-618.
97. Rost, B., and U. Riebesell 2004. Coccolithophores and the biological pump: responses to environmental changes. In H. R. Thierstein, and J. R. Young, eds. Coccolithophores: From Molecular Processes to Global Impact, pp. 99-125. Springer, Berlin.
98. Rost, B., U. Riebesell, S. Burkhardt, and D. Sültemeyer 2003. Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography 48:55-67.
99. Rost, B., U. Riebesell, and D. Sültemeyer 2006. Carbon acquisition of marine phytoplankton: effect of photoperiod length. Limnology and Oceanography 51:12-20.
100. Rost, B., I. Zondervan, and D. Wolf-Gladrow 2008. Sensitivity of phytoplankton to future changes in ocean carbonate chemistry: current knowledge, contradictions and research directions. Marine Ecology Progress Series 373:227-237.
101. Rynearson, T. A., and E. V. Armbrust 2000. DNA fingerprinting reveals extensive genetic diversity in a field population of the centric diatom Ditylum brightwellii. Limnology and Oceanography 45:1329-1340.
102. Rynearson, T. A., and E. V. Armbrust 2004. Genetic differentiation among populations of the planktonic marine diatom Ditylum brightwellii (Bacillariophyceae). Journal of Phycology 40:34-43.
103. Rynearson, T. A., and E. V. Armbrust 2005. Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii. Molecular Ecology 14:1631-1640.
104. Rynearson, T. A., J. A. Newton, and E. V. Armbrust 2006. Spring bloom development, genetic variation and population succession in the planktonic diatom Ditylum brightwellii. Limnology and Oceanography 51:1249-1261.
105. Schaum, E., B. Rost, A. J. Millar, and S. Collins 2013. Variation in plastic responses of a globally distributed picoplankton species to ocean acidification. Nature Climate Change 3:298-302.
106. Smayda, T. J. 1997. What is a bloom? A commentary. Limnology and Oceanography 42:1132-1136.
107. Smetacek, V. 1985. Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance. Marine Biology 84:239-251.
108. Steinacher, M., F. Joos, T. L. Frolicher, L. Bopp, P. Cadule, V. Cocco, S. C. Doney et al. 2010. Projected 21st century decrease in marine productivity: a multi-model analysis. Biogeosciences 7:979-1005.
109. 2 in a coastal dinoflagellate bloom: implications for interspecific competitive interactions and community structure. Evolutionary Biology 67:1879-1891.
110. Tatters, A. O., M. Y. Roleda, A. Schnetzer, F. Fu, C. L. Hurd, P. W. Boyd, D. A. Caron et al. 2013b. Short- and long-term conditioning of a temperate marine diatom community to acidification and warming. Philosophical Transactions of the Royal Society B: Biological Sciences 368:20120437.
111. Tortell, P. D., G. H. Rau, and F. M. M. Morel 2000. Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnology and Oceanography 45:1485-1500.
112. 2 sensitivity of Southern Ocean phytoplankton. Geophysical Research Letters 35:L4065.
113. Trimborn, S., D. Wolf-Gladrow, K.-U. Richter, and B. Rost 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.
114. Tyrrell, T., and A. Merico 2004. Emiliania huxleyi: bloom observations and the conditions that cause them. In H. R. Thierstein, and J. R. Young, eds. Coccolithophores: From Molecular Processes to Global Impact, pp. 75-97. Springer, Berlin.
115. 2: Natural Variations Archean to Present, pp. 99-110. AGU, Washington, DC.
116. Weynberg, K. D., M. J. Allen, K. Ashelford, D. J. Scanlan, and W. H. Wilson 2009. From small hosts come big viruses: the complete genome of a second Ostreococcus taurivirus, OtV-1. Environmental Microbiology 11:2821-2839.
117. Weynberg, K. D., M. J. Allen, I. C. Gilg, D. J. Scanlan, and W. H. Wilson 2011. Genome sequence of Ostreococcus tauri Virus OtV-2 throws light on the role of picoeukaryote niche separation in the ocean. Journal of Virology 85:4520-4529.
118. Winder, M., and U. Sommer 2012. Phytoplankton response to a changing climate. Hydrobiologia 698:5-16.
119. 2 concentration on growth and isotopic composition of marine plankton. Tellus B 51:461-476.