The possible evolution and future of CO2-concentrating mechanisms

Journal of Experimental Botany

Volumn 68, Issue 14, 2017, Pages 3701-3716

  Raven, John A ^a,b   Beardall, John ^c   Sánchez Baracaldo, Patricia ^d  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Algae; CO2 diffusion; CO2 concentrating mechanisms; Cyanobacteria; Evolution; Rubisco

Indexed keywords

ALGAL PROTEIN; BACTERIAL PROTEIN; CARBON DIOXIDE; PLANT PROTEIN; RIBULOSEBISPHOSPHATE CARBOXYLASE;

AUTOTROPHY; CARBON CYCLE; CLIMATE CHANGE; CYANOBACTERIUM; ENVIRONMENT; METABOLISM; MOLECULAR EVOLUTION; PLANT;

ALGAL PROTEINS; AUTOTROPHIC PROCESSES; BACTERIAL PROTEINS; CARBON CYCLE; CARBON DIOXIDE; CLIMATE CHANGE; CYANOBACTERIA; ENVIRONMENT; EVOLUTION, MOLECULAR; PLANT PROTEINS; PLANTS; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 85029459897     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erx110     Document Type: Review

References (201)

1. Abdul-Raman F, Petit E, Clanchard JL. 2013. The distribution of polyhedral bacterial microcompartments suggests frequent horizontal transfer and reassembly. Journal of Phylogenetics and Evolutionary Biology 1, 4.
2. Archer D, Eby M, Brovkon V, et al. 2009. Atmospheric lifetime of fossil fuel carbon dioxide. Annual Review of Earth and Planetary Sciences 37, 117-134.
3. Aubry S, Brown NJ, Hibberd JM. 2011. The role of proteins in C3 plants prior to their recruitment into the C4 pathway. Journal of Experimental Botany 62, 3049-3059.
4. Badger MR, Andrews TJ, Whitney SM, et al. 1998. The diversity and co-evolution of Rubisco, plastids, pyrenoids and chloroplast-based CO2 concentrating mechanisms in algae. Canadian Journal of Botany 76, 1052-1071.
5. Badger MR, Bek EJ. 2008. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. Journal of Experimental Botany 59, 1525-1541.
6. Badger MR, Hanson DT, Price GD. 2002. Evolution and diversity of CO2 concentrating mechanisms in cyanobacteria. Functional Plant Biology 29, 407-416.
7. Badger MR, Price GD. 2003. CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. Journal of Experimental Botany 54, 609-622.
8. Badger MR, Price GD, Long BM, Woodger FJ. 2006. The environmental plasticity and ecological genomics of the cyanobacterial CO2 concentrating mechanism. Journal of Experimental Botany 57, 249-265.
9. Barbour MM, Evans JR, Simonin KA, von Caemmerer S. 2016. Online CO2 and H2O oxygen isotope fractionation allows estimation of mesophyll conductance in C4 plants, and reveals that mesophyll conductance decreases as leaves age in both C4 and C3 plants. New Phytologist 210, 875-889.
10. Baurain D, Brinkmann H, Petersen J, Rodríguez-Ezpeleta N, Stechmann A, Demoulin V, Roger AJ, Burger G, Lang BF, Philippe H. 2010. Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Molecular Biology and Evolution 27, 1698-1709.
11. Beardall J. 1991. Effects of photon flux density on the 'CO2 concentrating mechanism' of the cyanobacterium Anabaena variabilis. Journal of Plankton Research 13, 133-142.
12. Beardall J, Giordano M. 2002. Ecological implications of microalgal and cyanobacterial CO2 concentrating mechanisms and their regulation. Functional Plant Biology 20, 335-340.
13. Beardall J, Griffiths H, Raven JA. 1982. Carbon isotope discrimination and the CO2 accumulating mechanism in Chlorella pyrenoidosa. Journal of Experimental Botany 33, 729-737.
14. Beardall J, Raven JA. 2016. Carbon acquisition by algae. In: Borowitzka M, Beardall J, Raven JA, eds. The physiology of microalgae. Heidelberg: Springer, 89-99.
15. Beardall J, Roberts S. 1999. Inorganic carbon acquisition by two species of Antarctic macroalgae: Porphyra endivifolium (Rhodophyta: Bangiales) and Palmaria decipiens (Rhodophyta: Palmariales). Polar Biology 21, 310-315.
16. Beardall J, Roberts S, Millhouse J. 1991. Effects of nitrogen limitation on uptake of inorganic carbon and specific activity of ribulose-1, 5- bisphosphate carboxylase-oxygenase in green microalgae. Canadian Journal of Botany 69, 1146-1150.
17. Beardall J, Roberts S, Raven JA. 2005. Regulation of inorganic carbon acquisition by phosphorus limitation in the green alga Chlorella emersonii. Canadian Journal of Botany 83, 859-864.
18. Beardall J, Stojkovic S, Gao K. 2014. Interactive effects of nutrient supply and other environmental factors on the sensitivity of marine primary producers to ultraviolet radiation: implications for the impacts of global change. Aquatic Biology 22, 5-23.
19. Bengtson S, Salistedt T, Belivanova V, Whitehouse M. 2017. Threedimensional preservation of cellular and subcellular structures suggests 1.6 billion-year-old crown-group red algae. PLoS Biology 15, e2000735.
20. Bermúdez R, Feng Y, Roleda MY, et al. 2015. Long-term conditioning to elevated pCO2 and warming influences the fatty acid and amino acid composition of the diatom Cylindrotheca fusiformis. PLoS One 10, e0123945.
21. Berner RA. 2004. The Phanerozoic carbon cycle: CO2 and O2. Oxford: Oxford University Press.
22. Berner RA. 2009. Phanerozoic atmospheric oxygen: new results using the GEOCARBSULF model. American Journal of Science 309, 603-606.
23. Bhatti S, Colman B. 2005. Inorganic carbon acquisition by the chrysophyte alga Mallomonas papillosa. Canadian Journal of Botany 83, 891-897.
24. Bhatti S, Colman B. 2008. Inorganic carbon acquisition in some synurophyte algae. Physiologia Plantarum 133, 33-40.
25. Bhatti S, Colman B. 2011. Evidence for the occurrence of photorespiration in synurophyte algae. Photosynthesis Research 109, 251-256.
26. Blank CE, Sánchez-Baracaldo P. 2010. Timing of morphological and ecological innovations in the cyanobacteria-a key to understanding the rise in atmospheric oxygen. Geobiology 8, 1-23.
27. Boller AR, Thomas PJ, Cavenaugh M, Scott KM. 2011. Low stable isotope fractionation by coccolithophore Rubisco. Geochimica et Geophysica Acta 75, 7200-7207.
28. Boller AJ, Thomas PJ, Cavanaugh CM, Scott KM. 2015. Isotopic discrimination and kinetic parameters of RubisCO from the marine bloomforming diatom, Skeletonema costatum. Geobiology 13, 33-43.
29. Bombar D, Heller P, Sánchez-Baracaldo P, Carter BJ, Zehr JP. 2014. Comparative genomics reveals surprising divergence of two closely related strains of uncultivated UCYN-A cyanobacteria. ISME Journal 8, 2530-2542.
30. Boyd PW, Cornwall CE, Davison A, Doney SC, Fourquez M, Hurd CL, Lima ID, McMinn A. 2016a. Biological responses to environmental heterogeneity under future ocean conditions. Global Change Biology 22, 2633-2650.
31. Boyd PW, Dillingham PW, McGraw CM, et al. 2016b. Physiological responses of a Southern Ocean diatom to complex future ocean conditions. Nature Climate Change 6, 207-213.
32. Breecker DO, Sharp ZD, McFadden LD. 2010. Atmospheric CO2 concentrations during ancient greenhouse climates were similar to those predicted for AD 2100. Proceedings of the National Academy of Sciences, USA 107, 575-580.
33. Brennan G, Collins S. 2015. Growth responses of a green alga to multiple environmental drivers. Nature Climate Change 5, 892-897.
34. Brodie J, Williamson CJ, Smale DA, et al. 2014. The future of the northeast Atlantic benthic flora in a high CO2 world. Ecology and Evolution 4, 2787-2798.
35. Brown JW, Sorhanus U. 2010. A molecular genetic timescale for the diversification of autotrophic stramenopiles (Ochrophyta): substantive underestimation of putative fossil ages. PLoS One 5, e12759.
36. Buchman N, Ehleringer JR. 1998. CO2 concentration profiles, and carbon and oxygen isotopes in C3 and C4 crop canopies. Agricultural and Forest Meteorology 89, 45-58.
37. Buick R. 1992. The antiquity of oxygenic photosynthesis: evidence from stromatolites in sulphate-deficient Archaean lakes. Science 255, 74-77.
38. Buick R. 2008. When did oxygenic photosynthesis evolve? Philosophical Transactions of the Royal Society B: Biological Sciences 363, 2731-2743.
39. Butterfield NJ. 2000. Bangiomorpha pubescens n.gen., n.sp.: implications for the evolution of sex, multicellularity, and mesoproterozoic/ neoproterozoic production of eukaryotes. Palaeobiology 26, 386-404.
40. Butterfield NJ. 2015. Proterozoic photosynthesis-a critical review. Palaeontology 58, 953-972.
41. Campbell AJ, Waddington ED, Warren SG. 2014. Refugium for surface life on Snowball Earth in a nearly enclosed sea? A numerical solution for sea-glacier invasion through a narrow strait. Journal of Geophysical Research: Oceans 119, 2679-2690.
42. Campbell L, Vaulot D. 1993. Photosynthetic picoplankton community structure in the subtropical North Pacific Ocean near Hawaii (Station Aloha). Deep Sea Research Part I Oceanographic Research Papers 48, 2043-2050.
43. Cardona T. 2015. A fresh look at the evolution and diversification of photochemical reaction centers. Photosynthesis Research 126, 111-134.
44. Casey JR, Lomas MW, Mandecki J, Walker DE. 2007. Prochlorococcus contributes to new production in the Sargasso Sea deep chlorophyll maximum. Geophysical Research Letters 34, L10604.
45. Chi S, Wu S, Wang K, Tang X, Liu T. 2014. Phylogeny of C4 photosynthesis enzymes based on algal transcriptomic and genomic data supports an archaeal/proteobacterial origin and multiple duplications for most C4 related genes. PLoS One 10, e110154.
46. Chrismas NA, Anesio AM, Sánchez-Baracaldo P. 2015. Phylogeny and diversity of cyanobacteria from extreme cold environments. Frontiers in Microbiology 6, 1070.
47. Chrismas NA, Barker G, Anesio AM, Sánchez-Baracaldo P. 2016. Genomic mechanisms for cold tolerance and production of exopolysaccharides in the Arctic cyanobacterium Phormidesmis priestleyi BC1401. BMC Genomics 17, 533.
48. Claire MW, Sheets J, Cohen M, et al. 2012. The evolution of solar flux from 0.1 nm to 160 μm: quantitative estimates for planetary studies. Astrophysical Journal 757, 95.
49. Clement R, Dimnet L, Maberly SC, Gontero B. 2016. The nature of the CO2-concentrating mechanisms in a marine diatom, Thalassiosira pseudonana. New Phytologist 209, 1417-1427.
50. Codispoti LA, Friederich GE, Hood DW. 1986. Variability of the inorganic carbon system over the SE Bering Sea during spring 1980 and spring-summer 1981. Continental Shelf Research 5, 133-160.
51. Codispoti LA, Friederich GE, Iverson RL, Hood DW. 1982. Temporal changes in the inorganic carbon system of the south-east Bering Sea during spring 1980. Nature 296, 242-245.
52. Collins S, Bell G. 2004. Phenotypic consequences of 1000 generations of selection at elevated CO2 in a green alga. Nature 431, 566-569.
53. Collins S, Bell G. 2006. Evolution of natural algal populations at elevated CO2. Ecology Letters 9, 129-135.
54. Cornejo-Castillo FM, Cabello AM, Salazar G, et al. 2016. Cyanobacterial symbionts diverged in the late Cretaceous towards lineagespecific nitrogen fixation factories in single-celled phytoplankton. Nature Communications 7, 11071.
55. Crawford RMM. 2014. Tundra-Taiga biology. Human, plant and animal survival in the Arctic. New York: Oxford University Press.
56. Delille B, Delille D, Fiala M, Prevost C, Frankignoule M. 2000. Seasonal changes of pCO2 over a subantarctic Macrocystis kelp bed. Polar Biology 23, 706-716.
57. Dillon JG, Castenholz RW. 1999. Scytonemin, a cyanobacterial sheath pigment, protects against UVC radiation: implications for early photosynthetic life. Journal of Phycology 35, 673-681.
58. Di Rienzi SC, Sharon I, Wrighton KC, et al. 2013. The human gut and groundwater harbor non-photosynthetic bacteria belonging to a new candidate phylum sibling to Cyanobacteria. Elife 1, e01102.
59. Doblin MA, van Sebille E. 2016. Drift in ocean currents impacts intergenerational exposure to temperature. Proceedings of the National Academy of Sciences, USA 113, 5700-5705.
60. Doney SC, Ruckelshaus M, Duffy JE, et al. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science 4, 11-37.
61. Edwards EJ, Still CJ. 2008. Climate, phylogeny and the ecological distribution of C4 grasses. Ecology Letters 11, 266-276.
62. Ehleringer JR, Sage RF, Flanagan LB, Pearcy RW. 1991. Climate change and the evolution of C4 photosynthesis. Trends in Ecology and Evolution 6, 95-99.
63. Eisenhut M, Ruth W, Haimovitch M, Bauwe H, Kaplan A, Hagemann M. 2008. The photorespiratory glycolate metabolism is essential for cyanobacteria and might have been conveyed endosymbiotically to plants. Proceedings of the National Academy of Sciences, USA 105, 17199-17204.
64. Fairchild IJ, Fleming EJ, Bao H, et al. 2015. Continental carbonate facies of a Neoproterozoic panglaciation, north-east Svalbard. Sedimentology 63, 443-497.
65. Field CB, Behrenfeld MJ, Randerson JT, Falkowski P. 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237-240.
66. Finkel ZV, Beardall J, Flynn KJ, et al. 2010. Phytoplankton in a changing world: cell size and chemical stoichiometry. Journal of Plankton Research 32, 119-137.
67. Fleming ED, Prufert-Bebout L. 2010. Characterization of cyanobacterial communities from high-elevation lakes in the Bolivian Andes. Journal of Geophysical Research Biogeosciences 115, G00D07.
68. Flynn KJ, Raven JA. 2017. What is the limit on photoautotrophic plankton growth rates? Journal of Plankton Research 39, 13-22.
69. Franks PJ, Royer DL, Beerling DJ, et al. 2014. New constraints on atmospheric CO2 concentration for the Phanerozoic. Geophysical Research Letters 41, 4685-4694.
70. Galmés J, Hermida-Carrera C, Laanisto L, Niinemets Ü. 2016. A compendium of temperature responses of Rubisco kinetic traits: variability among and within photosynthetic groups and impacts on photosynthesis modeling. Journal of Experimental Botany 67, 5067-5091.
71. Gao K, Helbling EW, Häder D-P, Hutchins DA. 2012. Responses of marine primary producers to interactions between ocean acidification, solar radiation and warming. Marine Ecology Progress Series 470, 167-189.
72. Genkov T, Meyer M, Griffiths H, Spreitzer RJ. 2010. Functional hybrid rubisco enzymes with plant small subunits and algal large subunits: engineered rbcS cDNA for expression in Chlamydomonas. Journal of Biological Chemistry 285, 19833-19841.
73. Giordano M, Norici A, Forssen M, Eriksson M, Raven JA. 2003. An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiology 132, 2126-2134.
74. Giordano M, Pezzoni V, Hell R. 2000. Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiology 124, 857-864.
75. Gonzalez-Esquer CR, Smarda J, Rippka R, Axen SD, Guglielmi G, Gugger M, Kerfeld CA. 2016. Cyanobacterial ultrastructure in light of genomic sequence data. Photosynthesis Research 129, 147-157.
76. Halevy I, Bachan A. 2017. The geologic history of seawater pH. Science 355, 1069-1071.
77. Harano K, Ishida H, Kittaka R, Kojima K, Inoue N, Tsukamoto M, Satoh R, Himeno M, Iwaki T, Wadano A. 2003. Regulation of the expression of ribulose-1, 5-bisphosphate carboxylase/oxygenase (EC 4.1.1.39) in a cyanobacterium, Synechococcus PCC7942. Photosynthesis Research 78, 59-65.
78. Henley SF, Annett AL, Ganeschram RS, et al. 2012. Factors influencing the stable carbon isotope composition of suspended and sinking organic matter in the coastal Antarctic sea ice environment. Biogeosciences 9, 1137-1157.
79. Hoffman PF. 2016. Cryoconite pans on Snowball Earth: supraglacial oases for Cryogenian eukaryotes? Geobiology 14, 531-542.
80. Hoffman PF, Schrag DP. 2002. The snowball Earth hypothesis: testing the limits of global change. Terra Nova 14, 129-155.
81. Hofmann HJ. 1976. Precambrian microflora, Belcher Islands, Canada: significance and systematics. Journal of Paleontology 50, 1040-1073.
82. Hopkinson BM, Young JN, Tansik AL, Binder BJ. 2014. The minimal CO2-concentrating mechanism of Prochlorococcus spp. MED4 is effective and efficient. Plant Physiology 166, 2205-2217.
83. Horath T, Bachofen R. 2009. Molecular characterization of an endolithic microbial community in dolomite rock in the central Alps (Switzerland). Microbial Ecology 58, 290-306.
84. Hu HH, Zhou QI. 2010. Regulation of inorganic carbon acquisition by nitrogen and phosphorus levels in Nannochloropsis sp. World Journal of Microbiology and Biotechnology 26, 957-961.
85. Hutchins DA, Walworth NG, Webb EA, Saito MA, Moran D, McIlvin MR, Gale J, Fu FX. 2015. Irreversibly increased nitrogen fixation in Trichodesmium experimentally adapted to elevated carbon dioxide. Nature Communications 6, 8155.
86. Johnson VR, Russell BD, Fabricius KE, Brownlee C, Hall-Spencer JM. 2012. Temperate and tropical brown macroalgae thrive, despite decalcification, along natural CO2 gradients. Global Change Biology 18, 2792-2803.
87. Johnston AM, Kennedy H. 1998. Carbon stable isotope fractionation in marine stems: open ocean studies and laboratory studies. In: Griffiths H, ed. Stable isotopes-integration of biological ecological and geochemical processes. Oxford: BIOS Scientific Publishers, 293-306.
88. Jordan DB, Ogren WL. 1981. Species variation in the specificity of ribulose bisphosphate carboxylase/oxygenase. Nature 291, 513-515.
89. Kah LC, Riding R. 2007. Mesoproterozoic carbon dioxide inferred from calcified cyanobacteria. Geology 35, 799-802.
90. Kapralov MV, Filatov DA. 2007. Widespread positive selection in the photosynthetic Rubisco enzyme. BMC Evolutionary Biology 7, 73.
91. Keeley JE. 1998. CAM photosynthesis in submerged aquatic plants. Botanical Review 64, 121-175.
92. Keeley JE, Keeley SC. 1989. Crassulacean acid metabolism (CAM) in high elevation tropical cactus. Plant, Cell and Environment 12, 331-336.
93. Kevekordes K, Holland D, Häubner N, et al. 2006. Inorganic carbon acquisition by eight species of Caulerpa (Caulerpaceae, Chlorophyta). Phycologia 45, 442-449.
94. Koch M, Bowes G, Ross C, Zhang XH. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19, 103-132.
95. Körner C. 1999. Alpine plant life. Functional plant ecology of high mountain ecosystems. Berlin: Springer.
96. Kozłowska-Szerenos B, Bialuk I, Maleszewski S. 2004. Enhancement of photosynthetic O2 evolution in Chlorella vulgaris under high light and increased CO2 concentration as a sign of acclimation to phosphate deficiency. Plant Physiology and Biochemistry 42, 403-409.
97. Kranz SA, Young JN, Hopkinson BM, Goldman JA, Tortell PD, Morel FM. 2015. Low temperature reduces the energetic requirement for the CO2 concentrating mechanism in diatoms. New Phytologist 205, 192-201.
98. Kronholm I, Collins S. 2016. Epigenetic mutations can both help and hinder adaptive evolution. Molecular Ecology 25, 1856-1868.
99. Ku SB, Edwards GE. 1977. Oxygen inhibition of photosynthesis: I. Temperature dependence and relation to O2/CO2 solubility ratio. Plant Physiology 59, 986-990.
100. Kubien DS, Sage RF. 2003. C4 grasses in boreal fens: their occurrence in relation to microsite characteristics. Oecologia 137, 330-337.
101. Kübler JE, Raven JA. 1995. The interaction between inorganic carbon supply and light supply in Palmaria palmata (Rhodophyta). Journal of Phycology 31, 369-375.
102. Kump LR. 2008. The rise of atmospheric oxygen. Nature 451, 277-278.
103. Lenton T, Daines S. 2017. Matworld-the biogeochemical effects of early life on land. New Phytologist (in press).
104. Lenton TM, Crouch M, Johnson M, et al. 2012. First plants cooled the Ordovician. Nature Geoscience 5, 86-89.
105. Letelier RM, Karl DM, Abbott MR, Bidigare RR. 2004. Light driven seasonal patterns of chlorophyll and nitrate in the lower euphotic zone of the North Pacific Subtropical Gyre. Limnology and Oceanography 49, 508-519.
106. Li F, Beardall J, Collins S, Gao K. 2016. Decreased photosynthesis and growth with reduced respiration in the model diatom Phaeodactylum tricornutum grown under elevated CO2 over 1800 generations. Global Change Biology 23, 127-137.
107. Li W, Gao K, Beardall J. 2012. Interactive effects of ocean acidification and nitrogen-limitation on the diatom Phaeodactylum tricornutum. PLoS One 7, e51590.
108. Lohbeck LT, Riebesell U, Reusch TBH. 2014. Gene expression changes in the coccolithophore Emiliania huxleyi after 500 generations of selection to ocean acidification. Proceedings of the Royal Society B: Biological Sciences 281, 2014003.
109. Losh JL, Young JN, Morel FM. 2013. Rubisco is a small fraction of total protein in marine phytoplankton. New Phytologist 198, 52-58.
110. Low-Décarie E, Jewell MD, Fussmann GF, Bell G. 2013. Long-term culture at elevated atmospheric CO2 fails to evoke specific adaptation in seven freshwater phytoplankton species. Proceedings of the Royal Society B: Biological Sciences 280, 2012590.
111. Lüttge U. 2004. Ecophysiology of crassulacean acid metabolism (CAM). Annals of Botany 93, 629-652.
112. Lyons TW, Reinhard CT, Planavsky NJ. 2014. Evolution: a fixednitrogen fix in the early ocean? Current Biology 24, R276-R278.
113. Maberly SC. 1996. Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshwater Biology 35, 579-598.
114. Maberly SC, Ball LA, Raven JA, Sültemeyer D. 2009. Inorganic carbon acquisition by chrysophytes. Journal of Phycology 45, 1052-1061.
115. Marconi M, Giordano M, Raven JA. 2011. Impact of taxonomy, geography, and depth on δ13C and δ15N variation in a large collection of macroalgae. Journal of Phycology 47, 1023-1035.
116. Mareš J, Hrouzek P, Kaňa R, Ventura S, Strunecký O, Komárek J. 2013. The primitive thylakoid-less cyanobacterium Gloeobacter is a common rock-dwelling organism. PLoS One 8, e66323.
117. McElwain JC, Montanez I, White JD, et al. 2016. Was atmospheric CO2 capped at 1000 ppm over the last 300 million years? Palaeogeography, Palaeoclimatology, Paleoecology 441, 653-658.
118. Meyer M, Griffiths H. 2013. Origins and diversity of eukaryotic CO2- concentrating mechanisms: lessons for the future. Journal of Experimental Botany 64, 769-786.
119. Mitchell C, Beardall J. 1996. Inorganic carbon uptake by an Antarctic sea-ice diatom Nitzchia frigida. Polar Biology 16, 95-99.
120. Mock T, Daines SJ, Geider R, Collins S, Metodiev M, Millar AJ, Moulton V, Lenton TM. 2016. Bridging the gap between omics and earth system science to better understand how environmental change impacts marine microbes. Global Change Biology 22, 61-75.
121. Murphy LR, Barrioca J, Franchschi VR, Lee R, Roalson EH, Edwards GE, Ku MSB. 2007. Diversity and plasticity of C4 photosynthesis in Eleocharis (Cyperaceae). Functional Plant Biology 34, 571-580.
122. Nakamura Y, Kaneko T, Sato S, et al. 2003. Complete genome structure of Gloeobacter violaceus PCC 7421, a cyanobacterium that lacks thylakoids. DNA Research 10, 137-145.
123. Nakayama T, Kamikawa R, Tanifuji G, et al. 2014. Complete genome of a non-photosynthetic cyanobacterium reveals recent adaptations to an intracellular lifestyle. Proceedings of the National Academy of Sciences, USA 111, 11407-11412.
124. Namsaraev Z, Mano NJ, Fernandez R, Wilmotte A. 2010. Biogeography of terrestrial cyanobacteria from Antarctic ice-free areas. Annals of Glaciology 51, 171-177.
125. Nienow JA, McKay CP, Friedmann EI. 1988. The cryptoendolithic microbial environment in the Ross Desert of Antarctica: light in the photosynthetically active region. Microbial Ecology 16, 271-289.
126. Oehler DZ. 1977. Pyrenoid-like structures in the late Precambrian algae from the bitter springs formation in Australia. Journal of Palaeontology 51, 885-901.
127. Olcott AN, Sessions AL, Corsetti FA, Kaufman AJ, de Oliviera TF. 2005. Biomarker evidence for photosynthesis during neoproterozoic glaciation. Science 310, 471-474.
128. Olson SL, Reinhard CT, Lyons TW. 2016. A limited role for methane in the mid-Proterozoic greenhouse. Proceedings of the National Academy of Sciences, USA 113, 11447-11452.
129. Olsson-Francis K, de la Torre R, Cockell CS. 2010. Isolation of novel extreme-tolerant cyanobacteria from a rock-dwelling microbial community by using exposure to low Earth orbit. Applied and Environmental Microbiology 76, 2115-2121.
130. Padfield D, Yvon-Durocher G, Buckling A, et al. 2016. Rapid evolution of metabolic traits explains thermal adaptation in phytoplankton. Ecology Letters 19, 133-142.
131. Pittermann J, Sage RF. 2001. The response of the high altitude C4 grass Muhlenbergia montana (Nutt.) A.S. Hitchc. to long- and short-term chilling. Journal of Experimental Botany 52, 829-838.
132. Porzio L, Buia MC, Hall-Spencer JM. 2011. Effects of ocean acidification on macroalgal communities. Journal of Experimental Marine Biology and Ecology 400, 278-287.
133. Porzio L, Garrard SL, Buia MC, Hall-Spencer JM. 2013. The effects of ocean acidification on early algal colonization stages at natural CO2 vents. Marine Biology 160, 2247-2259.
134. Price GD, Badger MR. 1989a. Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2- requiring phenotype: evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiology 91, 505-513.
135. Price GD, Badger MR. 1989b. Isolation and characterization of high CO2-requiring-mutants of the cyanobacterium Synechococcus PCC7942: two phenotypes that accumulate inorganic carbon but are apparently unable to generate CO2 within the carboxysome. Plant Physiology 91, 514-525.
136. Price GD, Badger MR, Woodger FJ, Long BM. 2008. Advances in understanding the cyanobacterial CO2-concentrating-mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. Journal of Experimental Botany 59, 1441-1461.
137. Pyankov VI, Black CC, Artyuschera EG, Vosnesenskaya EV, Ku MSB, Edwards GE. 1990. Features of photosynthesis in Haloxylon species of the Chenopodiaceae that are dominant plants in central Asian deserts. Plant and Cell Physiology 40, 125-134.
138. Pyankov VI, Voznesenskaya EV, Kuz'min AN, Ku MS, Ganko E, Franceschi VR, Black CC Jr, Edwards GE. 2000. Occurrence of C3 and C4 photosynthesis in cotyledons and leaves of Salsola species (Chenopodiaceae). Photosynthesis Research 63, 69-84.
139. Raven JA. 1997. The role of marine biota in the evolution of terrestrial biota: gases and genes. Biogeochemistry 39, 139-164.
140. Raven JA. 2009. Contributions of anoxygenic and oxygenic photolithotrophy and chemolithotrophy.to carbon and oxygen fluxes in aquatic systems. Aquatic Microbial Ecology 56, 177-192.
141. Raven JA. 2013. Rubisco: still the most abundant protein of Earth? New Phytologist 198, 1-3.
142. Raven JA, Ball LA, Beardall J, et al. 2005. Algae lacking carbonconcentrating mechanisms. Canadian Journal of Botany 83, 879-890.
143. Raven JA, Beardall J. 2014. CO2 concentrating mechanisms and environmental change. Aquatic Botany 118, 24-37.
144. Raven JA, Beardall J. 2016a. Algal photosynthesis and physiology. In: Slocombe SP, Benemann JR, eds. Microalgal production for biomass and high value products. Boca Raton, FL: CRC Press (Taylor and Francis Group), 1-19.
145. Raven JA, Beardall J. 2016b. The ins and outs of CO2. Journal of Experimental Botany 67, 1-13.
146. Raven JA, Giordano M. 2017. Acquisition and metabolism of carbon in the Ochrophyta other than diatoms. Philosophical Transactions of the Royal Society B: Biological Sciences (in press)
147. 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.
148. Raven JA, Johnston AM, Kübler JE, et al. 2002a. Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Functional Plant Biology 29, 355-378.
149. Raven JA, Johnston AM, Kübler JE, et al. 2002b. Seaweeds in cold seas: evolution and carbon acquisition. Annals of Botany 90, 525-536.
150. 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 UK 80, 1-25.
151. Retallack GJ, Gose BN, Osterhout JI. 2015. Periglacial paleosols and Cryogenian paleoclimate near Adelaide South Australia. Precambian Research 263, 1-18.
152. Reusch TB, Boyd PW. 2013. Experimental evolution meets marine phytoplankton. Evolution 67, 1849-1859.
153. Riding R. 2006. Cyanobacterial calcification, carbon dioxide concentrating mechanisms and Proterozoic-Cambrian changes in atmospheric composition. Geobiology 4, 283-298.
154. Royer DL. 2014. Atmospheric CO2 and O2 during the Phanorozoic: tools, patterns and impacts. In: Treatise on geochemistry, 2nd edn, Vol. 6. Amsterdam: Elsevier, 251-267.
155. Ruan Z, Giordano M, Raven JA. 2017. Energy partitioning between N assimilation and C acquisition and assimilation in energy and carbonlimited Synechococcus species. Journal of Experimental Botany 68 (in press).
156. Runcie JW, Gurgel CFD, McDermid KJ. 2008. In situ photosynthetic rates of tropical marine macroalgae at their lower depth limit. European Journal of Phycology 43, 377-388.
157. Sánchez-Baracaldo P. 2015. Origin of marine planktonic cyanobacteria. Scientific Reports 5, 17418.
158. Sánchez-Baracaldo P, Ridgwell A, Raven JA. 2014. A neoproterozoic transition in the marine nitrogen cycle. Current Biology 24, 652-657.
159. Saw JH, Schatz M, Brown MV, Kunkel DD, Foster JS, Shick H, Christensen S, Hou S, Wan X, Donachie SP. 2013. Cultivation and complete genome sequencing of Gloeobacter kilaueensis sp. nov., from a lava cave in Kilauea Caldera, Hawai'i. PLoS One 8, e76376.
160. Saxby-Rouen KJ, Leadbeater BSC, Reynolds CS. 1997. The growth response of Synura petersenii (Synurophyceae) to photon flux density, temperature and pH. Phycologia 36, 233-243.
161. Saxby-Rouen KJ, Leadbeater BSC, Reynolds CS. 1998. The relationship between growth of Synura petersenii (Synurophyceae) and components of the dissolved inorganic carbon system. Phycologia 37, 467-477.
162. Schaum CE, Collins S. 2014. Plasticity predicts evolution in a marine alga. Proceedings of the Royal Society B: Biological Sciences 281, 20141486.
163. Schaum CE, Rost B, Collins S. 2016. Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton. ISME Journal 10, 75-84.
164. Scheinin M, Riebesell U, Rynearson TA, et al. 2015. Experimental evolution gone wild. Journal of the Royal Society Interface 12, 20150056.
165. Schirrmeister BE, Gugger M, Donoghue PC. 2015. Cyanobacteria and the great oxidation event: evidence from genes and fossils. Palaeontology 58, 769-785.
166. Schirrmeister BE, Sánchez-Baracaldo P, Wacey D. 2016. Cyanobacterial evolution during the Precambrian. International Journal of Astrobiology 15, 187-204.
167. Schlüter L, Lohbeck KT, Gröger JP, Riebesell U, Reusch TB. 2016. Long-term dynamics of adaptive evolution in a globally important phytoplankton species to ocean acidification. Science Advances 2, e1501660.
168. Schlüter L, Lohbeck KT, Gutowska MA, et al. 2014. Adaptation of a globally important coccolithophore to ocean warming and acidification. Nature Climate Change 4, 1024-1030.
169. Scott KM, Henn-Sax M, Harmer YL, et al. 2007. Kinetic isotope effect and biochemical characterization of Form IA RubisCO from the marine cyanobacterium Prochlorococcus marinus MIT9313. Limnology and Oceanography 52, 2199-2204.
170. Sharkey TD, Berry JA. 1985. Carbon dioxide fractional of algae as influenced by an inducible CO2 concentrating mechanism. In: Lucas WJ, Berry JA, eds. Inorganic carbon uptake by aquatic organisms. Rockville, MD: American Society of Plant Physiologists, 389-401.
171. Shih PM, Occhialini A, Cameron JC, Andralojc PJ, Parry MA, Kerfeld CA. 2016. Biochemical characterization of predicted Precambrian RuBisCO. Nature Communications 7, 10382.
172. Smith RC, Marra J, Perry MJ, et al. 1989. Estimation of photon flux for the upper ocean in the Sargasso Sea. Limnology and Oceanography 34, 1675-1693.
173. Som SM, Buick R, Hagadorn JW, et al. 2016. Earth's air pressure 2.7 billion years ago constrained to less than half of present levels. Nature Geosciences 9, 448-451.
174. Soo RM, Skennerton CT, Sekiguchi Y, Imelfort M, Paech SJ, Dennis PG, Steen JA, Parks DH, Tyson GW, Hugenholtz P. 2014. An expanded genomic representation of the phylum cyanobacteria. Genome Biology and Evolution 6, 1031-1045.
175. Spijkerman E, Stojkovic S, Beardall J. 2014. CO2 acquisition in Chlamydomonas acidophila is influenced mainly by CO2, not phosphorus, availability. Photosynthesis Research 121, 213-221.
176. Stepien CC. 2015. Impacts of geography, taxonomy and functional group on inorganic carbon use patterns in marine macrophytes. Journal of Ecology 103, 1372-1383.
177. Stepien CC, Pfister CA, Wootton JT. 2016. Functional traits for carbon access in macrophytes. PLoS One 11, e0159062.
178. Still CJ, Berry JA, Collatz GJ, DeFries RS. 2003. Global distribution of C3 and C4 vegetation. Global Biogeochemical Cycles 17, 1006.
179. Strother PK, Battison L, Brasier MD, Wellman CH. 2011. Earth's earliest non-marine eukaryotes. Nature 473, 505-509.
180. Tcherkez GGB, Farquahar GD, Andrews TJ. 2006. Despite slow catalysis and confused substrate specificities, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proceedings of the National Academy of Sciences, USA 103, 7246-7251.
181. Trimborn S, Brenneis T, Sweet E, Rost B. 2013. Sensitivity of Antarctic phytoplankton species to ocean acidification. Growth, carbon acquisition and species interaction. Limnology and Oceanography 58, 997-1007.
182. Uemura K, Anwaruzzaman, Miyachi S, Yokota A. 1997. Ribulose-1, 5- bisphosphate carboxylase/oxygenase from thermophilic red algae with a strong specificity for CO2 fixation. Biochemical and Biophysical Research Communications 233, 568-571.
183. Ueno O, Samejima M, Muto S, Miyachi S. 1988. Photosynthetic characteristics of an amphibious plant, Eleocharis vivipara: expression of C4 and C3 modes in contrasting environments. Proceedings of the National Academy of Sciences, USA 85, 571-580.
184. Villareal JC, Renner SS. 2012. Hornwort pyrenoids, carbonconcentrating structures, evolved and were lost at least five times in the last 100 million years. Proceedings of the National Academy of Sciences, USA 109, 18873-19978.
185. Vincent WF, Gibson JA, Pienitz R, Villeneuve V, Broady PA, Hamilton PB, Howard-Williams C. 2000. Ice shelf microbial ecosystems in the high arctic and implications for life on snowball earth. Die Naturwissenschaften 87, 137-141.
186. Wacey D, Brasier M, Parnell J, et al. 2016. Contrasting microfossil preservation and lake chemistry with the 1200-1000 Ma Torridian supergroup of NW Scotland. In: Brasier AT, McInroy D, McLoughlin, eds. Earth system evolution and early life: a celebration of the work of Martin Brasier. London: Geological Society, Special Publication, 448.
187. Wallworth NG, Lee MD, Fu F-X, et al. 2016. Molecular and physiological evidence of genetic assimilation to high CO2 in the marine nitrogen fixer Trichodesmium. Proceedings of the National Academy of Sciences, USA 113, E7367-E7374.
188. Wang L, Yamano T, Kajikawa M, Hirono M, Fukuzawa H. 2014. Isolation and characterization of novel high-CO2-requiring mutants of Chlamydomonas reinhardtii. Photosynthesis Research 121, 175-184.
189. Wellman CH, Strother PK. 2015. The terrestrial biota prior to the origin of land plants (Embryophytes): a review of the evidence. Palaentology 58, 6501-627.
190. Wu Z, Zend B, Li R, Song L. 2012. Combined effects of carbon and phosphorus on the invasive cyanobacterium Cylindrospermopsis raciborski. Phycologia 51, 144-150.
191. Xu Z, Gao K. 2009. Impacts of UV radiation on growth and photosynthetic carbon assimilation in Gracilaria lemaneiformis (Rhodophyta) under phosphorus limited and replete conditions. Functional Plant Biology 36, 1057-1064.
192. Xu Z, Zou D, Gao K. 2010. Effects of elevated CO2 and phosphorus supply on growth, photosynthesis and nutrient uptake in the marine macroalga Gracilaria lemaneiformis (Rhodophyta). Botanica Marina 53, 123-129.
193. Yang EC, Boo GH, Kim HJ, Cho SM, Boo SM, Andersen RA, Yoon HS. 2012. Supermatrix data highlight the phylogenetic relationships of photosynthetic stramenopiles. Protist 163, 217-231.
194. Ye Q, Tong J, Zhu S, An J. 2015. The survival of benthic macroscopic phototrophs on a neoproterozoic snowball earth. Geology 43, 507-510.
195. Yokota A, Iwaki T, Miura K, et al. 1987. Model for the relationship between CO2-concentrating mechanism, CO2 fixation, and glycolate synthesis during photosynthesis in Chlamydomonas reinhardtii. Plant and Cell Physiology 28, 1363-1376.
196. Young EB, Beardall J. 2005. Modulation of photosynthesis and inorganic carbon acquisition in a marine microalga by nitrogen, iron and light availability. Canadian Journal of Botany 83, 917-928.
197. Young JN, Goldman JA, Kranz SA, Tortell PD, Morel FM. 2015b. Slow carboxylation of Rubisco constrains the rate of carbon fixation during Antarctic phytoplankton blooms. New Phytologist 205, 172-181.
198. Young JN, Heureux AM, Sharwood RE, Rickaby RE, Morel FM, Whitney SM. 2016. Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms. Journal of Experimental Botany 67, 3445-3456.
199. Young JN, Kranz SA, Goldman JAL, Tortell PD, Morel FMM. 2015a. Antarctic phytoplankton down-regulate their carbon-concentrating mechanisms under high CO2 with no change in growth rates. Marine Ecology Progress Series 532, 13-28.
200. Young JN, Rickaby RE, Kapralov MV, Filatov DA. 2012. Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 483-492.
201. Zehr JP, Bench SR, Carter 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.