CO2 concentrating mechanisms in algae: Mechanisms, environmental modulation, and evolution

Annual Review of Plant Biology

Volumn 56, Issue , 2005, Pages 99-131

  Giordano, Mario ^a   Beardall, John ^b   Raven, John A ^c  

^a UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Carbonic anhydrase; Carboxysome; Cyanobacteria; Inorganic carbon; Photosynthesis; Pyrenoid

Indexed keywords

ALGAE; CYANOBACTERIA; EMBRYOPHYTA;

CARBON DIOXIDE; CARBONATE DEHYDRATASE;

ALGA; CYANOBACTERIUM; ENVIRONMENT; ENZYMOLOGY; EVOLUTION; METABOLISM; PHOTOSYNTHESIS; REVIEW;

ALGAE; CARBON DIOXIDE; CARBONIC ANHYDRASES; CYANOBACTERIA; ENVIRONMENT; EVOLUTION; PHOTOSYNTHESIS;

EID: 20444389072     PISSN: 15435008     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.arplant.56.032604.144052     Document Type: Review

References (215)

1. Allemand D, Furia P, Bénazet-Tambutté S. 1998. Mechanisms of carbon acquisition for endosymbiont photosynthesis in Anthozoa. Can. J. Bot. 76:925-41
2. 2 in cells and chloroplasts from the microalgae Chlamydomonas reinhardtii and Dunaliella tertiolecta. Plant Physiol. 116:193-201
3. Ananyev GM, Zoltsman L, Vasko C, Dismukes GC. 2001. The inorganic biochemistry of photosynthetic oxygen evolution/water oxidation. Biochim. Biophys. Acta 1503:52-68
4. Arancibia-Avila P, Coleman JR, Russin WA, Graham JM, Graham LE. 2001. Carbonic anhydrase localization in charophycean green algae: ecological and evolutionary significance. Int. J. Plant. Sci. 162:127-35
5. Ashida H, Saito Y, Kojima C, Kobayashi K, Ogasawara N, et al. 2003. A functional link between RuBisCO-like protein of Bacillus and photosynthetic RuBisCO. Science 302:286-90
6. 2 concentrating mechanisms. Photosynth. Res. 77:83-94
7. 2-concentrating mechanisms in the algae. Can. J. Bot. 76:1052-71
8. - accumulation by the cyanobacterium Synechococcus PCC6301 to growth at different inorganic carbon concentrations. Aust. J. Plant Physiol. 14:189-201
9. 2 concentrating mechanisms in cyanobacteria. Funct. Plant Biol. 29:161-73
10. - fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol. Plant. 90:529-36
11. 2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J. Exp. Bot. 54:609-22
12. Ball LA. 2003. Carbon acquisition in the chrysophyte algae. PhD thesis. Univ. Dundee, xv + 270 pp.
13. 2 concentrating mechanism" of the cyanobacterium Anabaena variabilis. J. Plankton Res. 13:133-41
14. Beardall J, Giordano M. 2002. Ecological implications of microalgal and cyanobacterial CCMs and their regulation. Funct. Plant Biol. 29:335-47
15. 2 accumulating mechanism in Chlorella emersonii. J. Exp. Bot. 33:729-37
16. Beardall J, Heraud P, Roberts S, Shelly K, Stojkovic S. 2002. Effects of UV-B radiation on inorganic carbon acquisition by the marine microalga Dunalietta tertiolecta (Chlorophyceae). Phycologia 41:268-72
17. 2 concentrating mechanism in cyanobacteria and microalgae. Can. J. Bot. 76:1010-17
18. Beardall J, Mukerji D, Glover HE, Morris I. 1976. The path of carbon in photosynthesis by marine phytoplankton. J. Phycol. 12:409-17
19. Beardall J, Quigg AS, Raven JA. 2003. Oxygen consumption: photorespiration and chlororespiration. In Photosynthesis in Algae, ed. AWD Larkum, SE Douglas, JA Raven, pp. 157-81. Dordrecht, The Netherlands: Kluwer
20. Beardall J, Raven JA. 2004. The potential effects of global climate change on microalgal photosynthesis, growth and ecology. Phycologia 43:31-45
21. 2 carboxylase in green microalgae. Can. J. Bot. 69:1146-50
22. 21a. Beardall J, Roberts S, Raven JA. 2005. Regulation of inorganic carbon acquisition by phosphorus limitation in the green alga Chlorella emersonii. Can. J. Bot. In press
23. Behrenfeld MJ, Bale A, Kolber ZS, Aiken J, Falkowski PG. 1996. Confirmation of iron limitation of phytoplankton photosynthesis in the equatorial Pacific Ocean. Nature 383:508-11
24. Behrenfeld MJ, Randerson JT, McClain CR, Feldman GC, Los SO, et al. 2001. Biospheric primary production during an ENSO transition. Science 291:2594-97
25. Bekker A, Holland HD, Wang PL, Rumble D, Stein HJ, et al. 2004. Dating the rise of atmospheric oxygen. Nature 427:117-20
26. Berman-Frank I, Kaplan A, Zohary T, Dubinsky Z.1995. Carbonic anhydrase activity in the bloom-forming dinoflagellate Peridinium gatunense. J. Phycol. 31:906-13
27. Bertilsson S, Berglund O, Karl DM, Chisholm SW. 2003. Elemental composition of marine Prochlococcus and Synechococcus: implications for the ecological stoichiometry of the sea. Limnol. Oceanogr. 48:1721-31
28. Bhatti S, Huertas IE, Colman B. 2002. Acquisition of inorganic carbon by the marine haptophyte Isochrysis galbana (Prymnesiophyceae). J. Phycol. 38:914-21
29. 2 across the human erythrocyte membrane. J. Physiol. 550:419-29
30. 2 concentration in the green alga Chlorella kessleri. J. Exp. Bot. 51:1341-48
31. Brocks JJ, Logan GA, Buick R, Summons RE. 1999. Archean molecular fossils and the early rise of eukaryotes. Science 285:1033-36
32. 2 concentrations. Limnol. Oceanogr. 46:1378-91
33. Burns DB, Beardall J. 1987. Utilization of inorganic carbon by marine microalgae. J. Exp. Mar. Biol. Ecol. 107:75-86
34. Busch S, Schmidt R. 2001. Enzymes associated with the β-carboxylation pathway in Ectocarpus siliculosus (Phaeophyceae): Are they involved in net carbon acquisition? Eur. J. Phycol. 36:61-70
35. Butterfield NJ. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the mesoproterozoic/neoproterozoic radiation of eukaryotes. Palaeobiology 26:386-404
36. Calamita G, Kempf B, Rudd KE, Bonhivers M, Kneip S, et al. 1997. The aquaporin-Zwater channel gene of Escherichia coli: structure, organization and phylogeny. Biol. Cell 85:321-29
37. Cannon GC, Bradburne CE, Aldrich HC, Baker SH, Heinhorst S, Shively JM. 2001. Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl. Environ. Microbiol. 67:5351-61
38. Colman B, Huertas IE, Bhatti S, Dason JS. 2002. The diversity of inorganic carbon acquisition mechanisms in eukaryotic microalgae. Funct. Plant Biol. 29:261-70
39. Cram WJ. 1974. Influx isotherms - their interpretation and use. In Membrane Transport in Plants, ed. U Zimmermann, J Dainty, pp. 334-37. Berlin: Springer-Verlag
40. 2 concentration. Nature 402:165-67
41. Dason JS, Huertas IE, Colman B. 2004. Source of inorganic carbon for photosynthesis in two marine dinoflagellates. J. Phycol. 40:285-92
42. Davies JP, Grossman AR. 1998. Responses to deficiencies in macronutrients. In The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomanas. ed. J-D Rochaix, M Golschmidt-Clermont, S Merchant, pp. 613-33. Amsterdam: Kluwer
43. Davies JP, Yildiz FH, Grossman AR. 1996. Sad, a putative regulator that is critical to survival of Chlamydomonas reinhardtii during sulfur deprivation. EMBO J. 15:2150-59
44. Dufresne A, Salanoubat M, Partensky F, Artiguenave F, Axmann IM, et al. 2003. Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc. Nat. Acad. Sci. USA 100:10020-25
45. El Alaoui S, Diez J, Toribio F, Gomez-Baena G, Dufresne A, Garcia-Fernandez JM. 2003. Glutamine synthetase from the marine cyanobacteria Prochlorococcus spp.: characterization, phylogeny and response to nutrient limitation. Environ. Microbiol. 5:412-23
46. Elzenega JTM, Prins HBA, Stefels J. 2000. The role of extracellular carbonic anhydrase activity in inorganic carbon utilization of Phaeocystis globosa (Prymnesiophyceae): a comparison with other marine algae using the isotopic disequilibrium technique. Limnol. Oceanogr. 45:372-80
47. 2-induced polypeptide in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 93:12031-34
48. Falkowski PG, Katz ME, Knoll AH, Quigg A, Raven JA, et al. 2004. The evolution of modern eukaryotic phytoplankton. Science 305:354-60
49. Falkowski PG, Raven JA. 1997. Aquatic Photosynthesis. Malden, MA: Blackwell Sci.
50. II protein in Synechococcus PCC 7942 senses and signals 2-oxoglutarate under ATP-replete conditions. In The Phototrophic Prokaryotes, ed. W Löffelhardt, G Schmetterer, GA Peschek, pp. 549-53. New York: Kluwer Plenum
51. Fujiwara S, Fukuzawa H, Tachiki A, Miyachi S. 1990. Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. Proc. Natl. Acad. Sci. USA 87:9779-83
52. 2 concentration. Proc. Natl. Acad. Sci. USA 87:4383-87
53. 2 availability. Proc. Natl. Acad. Sci. USA 98:5347-52
54. Furla P, Bénazet-Tambatté S, Allemand D. 1998. Functional polarity of the tentacle of the sea anemone Anemonia viridis: role in inorganic carbon acquisition. Am. J. Physiol. 274:R303-10
55. Geider RJ, LaRoche J, Greene RM, Olaizola M. 1993. Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J. Phycol. 29:755-66
56. Geider RJ, MacIntyre HL, Graziano LM, McKay RML. 1998. Responses of the photosynthetic apparatus of Dunaliella tertiolecta (Chlorophyceae) to nitrogen and phosphorus limitation. Eur. J. Phycol. 33:315-32
57. 2: a possible mitochondrial role in adaptation. Plant Physiol. 111:1339-47
58. 2 and high N concentrations. J. Plant Physiol. 158 (5):577-81
59. 2 concentration and nitrogen source used for growth. Plant Physiol. 115:1049-56
60. Giordano M, Hell R. 2001. Mineral nutrition in photolithotrophs: cellular mechanisms controlling growth in terrestrial and aquatic habitats. Recent Res. Dev. Plant Physiol. 2:95-123
61. Giordano M, Norici A, Forssen M, Eriksson M, Raven JA. 2003. An anaplerotic role for mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol. 132:2126-34
62. Giordano M, Pezzoni V, Hell R. 2000. Strategies for the allocation of resources under sulfur limitation in the green alga Dunaliella salina. Plant Physiol. 124:857-64
63. Graur D, Martin W. 2004. Reading the entrails of chickens: molecular timescales of evolution and the illusion of precision. Trends Genet. 20:80-86
64. Green BJ, Li W-Y, Manhart JR, Fox TC, Summer EJ, et al. 2000. Mollusc-algal chloroplast endosymnbiosis. Photosynthesis, thylakoid maintenance, and chloroplast gene expression continues for many months in the absence of the algal nucleus. Plant Physiol. 124:331-42
65. Greene RM, Geider RJ, Kolber Z, Falkowski PG. 1992. Iron-induced changes in light harvesting and photochemical energy conversion processes in eukaryotic marine algae. Plant Physiol. 100:565-75
66. 13C in marine organic matter and isotopic fractionation in the global biogeochemical cycle of carbon during the last 800 Ma. Chem. Geol. 161:103-25
67. Heldal M, Scanlan DJ, Norland S, Thingstad F, Mann NH. 2003. Elemental composition of single cells of various strains of marine Prochlorococcus and Synechococcus using X-ray microanalysis. Limnol. Oceanogr. 48:1732-43
68. Hessler AM, Lowe DR, Jones RL, Bird DK. 2004. A lower limit for atmospheric carbon dioxide levels 3.2 billion years ago. Nature 428:736-38
69. Higgins CF. 2001. ABC transporters: physiology, structure and mechanism - an overview. Res. Microbiol. 152:205-10
70. Hillrichs S, Schmid R. 2001. Activation by blue light of inorganic carbon acquisition for photosynthesis in Ectocarpus siliculosus: organic acid pools and short-term carbon fixation. Eur. J. Phycol. 36:71-79
71. Hiltonen T, Björkbacka H, Forsman C, Clarke AK, Samuelsson G. 1998. Intracellular β-carbonic anhydrase of the unicellular green alga Coccomyxa. Cloning of the cDNA and characterization of the functional enzyme overexpressed in Escherichia coli. Plant Physiol. 117:1341-49
72. Hisbergues M, Jeanjean R, Joset F, Tandeau de Marsac N, Bedu S. 1999. Protein PII regulates both inorganic carbon and nitrate uptake and is modified by a redox signal in Synechocystis PCC 6803. FEBS Lett. 463:216-20
73. Huertas IE, Bhatti S, Colman B. 2003. Inorganic carbon acquisition in two species of prymnesiophytes. Eur. J. Phycol. 38:181-89
74. Huertas IE, Colman B, Espie GS. 2002. Inorganic carbon acquisition and its energization in eustigmatophyte algae. Funct. Plant Biol. 29:271-77
75. 2 by three species of marine microalgae. J. Phycol. 36:314-20
76. 2 efflux in the marine microalga Nannochloropsis gaditana. Planta 211:43-49
77. Huertas IE, Lubian LL. 1998. Comparative study of dissolved inorganic carbon utilization and photosynthetic responses in Nannochloris (Chlorophyceae) and Nannochloropsis (Eustigmatophyceae) species. Can. J. Bot. 76 : 1104-08
78. Im CS, Grossman AR. 2001. Identification and regulation of high light-induced genes in Chlamydomonas reinhardtii. Plant J. 30:301-13
79. II in Synechococcus PCC7942: identification of an ATP and 2-oxoglutarate-regulated phosphatase activity. Mol. Microbiol. 26:81-90
80. Johnson KS. 1981. Carbon dioxide hydration and dehydration kinetics in seawater. Limnol. Oceanogr. 27:849-55
81. Johnston AM. 1991. The acquisition of inorganic carbon by marine macroalgae. Can. J. Bot. 69:1123-32
82. 4 photosynthesis in a marine diatom. Nature 412:40-41
83. Kaplan A, Lieman-Hurwitz J, Tchernov D. 2004. Resolving the biological role of the Rhesus (Rh) proteins of red blood cells with the aid of a green alga. Proc. Natl. Acad. Sci. USA 101:7497-98
84. 2 concentrating mechanisms in photosynthetic microorganisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:539-59
85. 2. EMBO J. 17:1208-16
86. Kasting JF, Catling D. 2003. Evolution of a habitable planet. Annu. Rev. Astron. Astrophys. 41:429-63
87. Keeley JE. 1996. Aquatic photosynthesis. In Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution, ed. K Winter, JAC Smith, pp. 281-95. Berlin: Springer-Verlag
88. 4 carbon-concentrating mechanisms. Int. J. Plant Sci. 164:S55-S77
89. 2 uptake in Synechoccus sp. PCC7002 gives evidence for multiple NDH-1 complexes with specific roles in cyanobacteria. Mol. Microbiol. 32:1305-15
90. Korb RE, Saville PJ, Johnston AM, Raven JA. 1997. Sources of inorganic carbon for photosynthesis by three species of marine diatom. J. Phycol. 33:433-40
91. Kübler JE, Raven JA. 1994. Consequences of light-limitation for carbon acquisition in three rhodophytes. Mar. Ecol. Pogr. Ser. 110:203-8
92. Kübler JE, Raven JA. 1995. The interaction between inorganic carbon supply and light supply in Palmaria palmata (Rhodophyta). J. Phycol. 31:369-75
93. 2 concentration during growth of Chlamydomonas reinhardtii: independent regulation of pyrenoid starch and stroma starch. Plant Cell Physiol. 29:1269-78
94. Lane TW, Morel FMM. 2000. Regulation of carbonic anhydrase expression by zinc, cobalt and carbon dioxide in the marine diatom Thalassiosira weissflogii. Plant Physiol. 123:345-52
95. Lane TW, Morel FMM. 2000. A biological function for cadmium in marine diatoms. Proc. Natl. Acad. Sci. USA 97:4627-31
96. Larsson C, Axelsson L. 1999. Bicarbonate uptake and utilization in marine macroalgae. Eur. J. Phycol. 34:79-86
97. Lee H-M, Flores E, Herrero A, Houmard J, Tandeau de Marsac N. 1998. A role for the signal transduction protein PII in the control of nitrate/nitrite uptake in a cyanobacterium. FEBS Lett. 427:291-95
98. II (GlnB) and influences its phosphorylation level in response to nitrogen and carbon supplies in the cyanobacterium Synechococcus sp. strain PCC 7942. J. Bacteriol. 181:2697-702
99. 2 concentrations. Protist 149:341-45
100. 2 and the timing of evolution of secondary endosymbioses. Phycologia 39:167-72
101. Ludwig M, Sültemeyer D, Price GD. 2000. Isolation of ccmKLMN genes from the marine cyanobacterium Synechococcus sp. PCC7002 (cyanobacteria), and evidence that ccmM is essential for carboxysome assembly. J. Phycol. 36:1109-18
102. Maberly SC. 1996. Diel, episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshwater Biol. 35:579-98
103. MacFarlane JJ, Raven JA. 1990. C, N and P nutrition of Lemanea mammilosa Kütz. (Batrachospermales, Rhodophyta) in the Dighty Burn, Angus, Scotland. Plant Cell Environ. 13:1-13
104. 2 hydration in the cyanobacterium Synechococcus sp. PCC7942. Mol. Microbiol. 43:425-36
105. Maeda S, Price GD, Badger MR, Enomoto C, Omata T. 2000. Bicarbonate binding activity of the CmpA protein of the cyanbacterium Synechococcus sp strain PCC 7942 involved in active transport of bicarbonate. J. Biol. Chem. 275:20551-55
106. Maeda S, Omata T. 1997. Substrate-binding lipoprotein of the cyanobacterium Synechococcus sp. Strain PCC 7942 involved in the transport of nitrate and nitrite. J. Biol. Chem. 272:3036-41
107. 2. Plant Physiol. 88:491-96
108. Marcus Y, Berry JA, Pierce J. 1992. Photosynthesis and photorespiration in a mutant of the cyanobacterium Synechocystis PCC 6803 lacking carboxysomes. Planta 187:511-16
109. Martin W, Rujan T, Richley E, Hansen A, Cornelson S, et al. 2002. Evolutionary analysis of Arabidopsis, cyanobacterial and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl. Acad. Sci. USA 99:12246-51
110. 2 concentration. Plant Physiol. 108:253-60
111. 2. J. Exp. Bot. 47:1951-56
112. 2 in the marine alga Phaeodactylum tricornutum. Plant Cell Environ. 24:611-20
113. 2 concentration in the diatom Phaeodactylum sp. Funct. Plant Biol. 29:279-87
114. Matsuzaki M, Misumu O, Shin-I T, Maruyama M, Miyagishima SY, et al. 2004. Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653-57
115. Mayo WP, Williams TG, Birch DG, Turpin DH. 1986. Photosynthetic adaptation by Synechococcus leopoliensis in response to exogenous dissolved inorganic carbon. Plant Physiol. 80:1038-40
116. 2-concentrating mechanism in Synechocystis sp. PCC6803. Plant Cell Environ. 27:615-26
117. + requirement for growth, photosynthesis, and pH regulation in the alkalotolerant cyanobacterium Synechococcus leopoliensis. J. Bacteriol. 159:100-6
118. --limited chemostats. Plant Physiol. 75:1064-70
119. Mitchell C, Beardall J. 1996. Inorganic carbon uptake by an Antarctic sea-ice diatom Nitzchia frigida. Polar Biol. 16:95-99
120. Mitra M, Lato SM, Ynalvez RA, Xiao Y, Moroney JV. 2004. Identification of a new chloroplast carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol. 135:173-82
121. Morel FMM, Cox EH, Kraepiel AML, Lane TW, Milligan AJ, et al. 2002. Acquisition of inorganic carbon by the marine diatom Thalassiosira weissflogii. Funct. Plant Biol. 29:301-8
122. 2-concentrating mechanism in some species of the pyrenoid-less free-living algal genus Chloromonas (Volvocales, Chlorophyta). Planta 204:269-76
123. 2-concentrating mechanism: comparative morphology, physiology and molecular phylogenetic analysis of closely related strains of Chlamydomonas and Chloromonas. Planta 208:365-72
124. Moroney JV, Bartlett SG, Samuelsson G. 2001. Carbonic anhydrases in plants and algae. Plant Cell Environ. 24:141-53
125. Moroney JV, Chen ZY. 1998. The role of the chloroplast in inorganic carbon uptake by eukaryotic algae. Can. J. Bot. 76:1025-34
126. Morris I, Beardall J, Mukerji D. 1978. The mechanisms of carbon fixation in phytoplankton. Mitt. Internat. Verein. Limnol. 21:174-83
127. Muro-Pastor MI, Reyes JC, Florencio FJ. 2001. Cyanobacteria perceive nitrogen status by sensing intracellular 2-oxoglutarate. J. Biol. Chem. 276:38320-28
128. 2 permeability of Xenopus oocyte? Am. J. Physiol. 274:C543-48
129. Ogawa T, Miyano A, Inoue Y. 1985. Photosystem-I-driven inorganic carbon transport in the cyanobacterium, Anacystis nidulans. Biochim. Biopbys. Acta. 808:74-75
130. Ogawa T, Ogren WL. 1985. Action spectra for accumulation of inorganic carbon in the cyanobacterium, Anabaena variabilis. Photochem. Photobiol. 41:583-87
131. Ohkawa H, Pakrasi HB, Ogawa T. 2000. Two types of functionally distinct NAD(P)H dehydrogenases in Synechocystis sp strain PCC6803. J. Biol. Chem. 275:31630-34
132. - uptake in Synechocystis sp strain PCC 6803. J. Bacteriol. 182:2591-96
133. Omata T, Price GD, Badger MR, Okamura M, Gohta S, Ogawa T. 1999. Identification of an ATP-binding cassette transporter involved in bicarbonate uptake in the cyanobacterium Synechococcus sp. Strain. Proc. Natl. Acad. Sci. USA 96:13571-756
134. Palinska KA, Laloui W, Bèdu S, Loiseaux-de Goër S, Castets AM, et al. 2002. The signal transducer PII and bicarbonate acquisition in Prochlorococcus marinus PCC 9511, a marine cyanobacterium naturally deficient in nitrate and nitrite assimilation. Microbiol. 148:2405-12
135. Palmqvist K. 2000. Carbon economy in lichens. New Phytol. 148:11-36
136. Palmqvist K, Sundblad L-G, Wingsle G, Samuelsson G. 1990. Acclimation of photosynthetic light reactions during induction of inorganic carbon accumulation in the green alga Chlamydomonas reinhardtii. Plant Physiol. 94:357-66
137. Palmqvist K, Yu J-W, Badger MR. 1994. Carbonic anhydrase activity and inorganic carbon fluxes in low- and high-Ci cells of Chlamydomonas reinhardtii and Scenedesmus obliquus. Physiol. Plant. 90:537-47
138. 2 concentrating mechanism. Plant Physiol. 91:505-13
139. Price GD, Maeda S, Omata T, Badger M. 2002. Modes of active inorganic carbon uptake in the cyanobacterium Synechococcus sp. PCC7942. Funct. Plant Biol. 29:131-49
140. 2 concentration mechanism: investigation by means of photosystem-deficient and carbonic anhydrase-deficient mutants of Chlamydomonas reinhardtii. Photosynthetica 28:515-22
141. Pronina NA, Semenenko VE. 1984. Localisation of membrane bound and soluble carbonic anhydrase in the Chlorella cell. Fiziologia Rastenii 31:241-51
142. 2 in the chloroplast of microalgae. Sov. Plant Physiol. 39:470-76
143. 2-concentrating mechanism is correlated with the formation of the starch sheath around the pyrenoid of Chlamydomonas reinhardtii. Planta 195:210-16
144. 2 and temperature. Plant Cell Environ. 14:779-94
145. 2 episodes. Palaeogeogr. Palaeoclimatol. Palaeoecol. (Glob. Planet. Chang. Sect.) 97:19-38
146. Raven JA. 1997. Putting the C in phycology. Eur. J. Phycol. 32:319-33
147. Raven JA. 1997. Inorganic carbon acquisition by marine autotrophs. Adv. Bot. Res. 27:85-209
148. 2 concentrating mechanisms: a role for thylakoid lumen acidification? Plant Cell Environ. 20:147-54
149. Raven JA. 2000. Land plant biochemistry. Phil. Trans. Roy. Soc. Lond. B. 355:833-45
150. 2-grown cells of Chlamydomonas reinhardtii. Plant Cell Environ. 24:261-65
151. Raven JA. 2003. Carboxysomes and peptidoglycan walls of cyanelles: possible physiological functions. Eur. J. Phycol. 38:47-53
152. Raven JA. 2003. Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynth. Res. 77:155-71
153. Raven JA, Beardall J. 1981. Carbon dioxide as the exogenous inorganic carbon source for Batrachospermum and Lemanea. Br. Phycol. J. 16:165-75
154. Raven JA, Beardall J. 2003. Carbon acquisition mechanisms in algae: carbon dioxide diffusion and carbon dioxide concentrating mechanisms. In Photosynthesis in Algae, ed. AWD Larkum, SE Douglas, JA Raven, pp. 225-44. Dordrecht, The Netherlands: Kluwer
155. Raven JA, Beardall J, Griffiths H. 1982. Inorganic C sources for Lemanea, Cladophora and Ranunculus in a fast-flowing stream: measurements of gas exchange and of carbon isotope ratio and their ecological implications. Oecologia 53:68-78
156. Raven JA, Beardall J, Johnston AM, Kübler J, Geoghegan I. 1995. Inorganic carbon acquisition by Hormosira banksii (Phaeophyta: Fucales) and its epiphyte Notheia anomala (Phaeophyta: Fucales). Phycologia 34:267-77
157. Raven JA, Beardall J, Johnston AM, Kübler JE, McInroy S. 1996. Inorganic carbon acquisition by Xiphophora chondrophylla (Phaeophyta: Fucales). Phycologia. 35:83-89
158. Raven JA, Johnston AM, Kübler JE, Korb J, McInroy SG, et al. 2002. Seaweeds in cold seas: evolution and carbon acquisition. Ann. Bot. 90:525-36
159. Raven JA, Johnston AM, Kübler JE, Korb RE, McInroy SG, et al. 2002. Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and seagrasses. Funct. Plant Biol. 29:355-78
160. Raven JA, Kübler JE, Beardall J. 2000. Put out the light and then put out the light. J. Mar. Biol. Assoc. UK 80:1-25
161. 2 by aquatic vegetation. Plant Cell Environ. 8:417-25
162. Raven JA, Walker DI, Jensen KR, Handley LL, Scrimgeour CM, et al. 2001. What fraction of the organic carbon in saccoglosan is obtained from photosynthesis by kleptoplastids? An investigation using the natural abundance of stable isotopes. Mar. Biol. 138:537-45
163. Rawat M, Moroney JV. 1991. Partial characterization of a new isozyme of carbonic anhydrase isolated from Chlamydomonas reinhardtii. J. Biol. Chem. 266:9719-23
164. 4 photosynthesis in a marine diatom. Nature 407:996-99
165. 4 photosynthesis in carbon accumulation and fixation in a marine diatom. Plant Physiol. 135:2106-11
166. 4-like photosynthetic characteristics. Proc. Natl. Acad. Sci. USA 88:2883-87
167. Reiskind JB, Seaman PT, Bowes G. 1988. Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiol. 87:686-92
168. Ritchie RJ, Nadolny C, Larkum AWD. 1996. Driving forces for bicarbonate transport in the cyanobacterium Synechococcus R-Z (PCC 7942). Plant Physiol. 112:1573-84
169. Roberts S, Beardall J. 1999. Inorganic carbon acquisition by two species of Antarctic macroalgae: Porphyra endivifolium (Rhodophyta: Bangiales) and Palmaria decipiens (Rhodophyta: Palmariales). Polar Biol. 21:310-15
170. Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, et al. 2003. Genome divergence in two Prochlorococcus ecotypes reflects niche differentiation. Nature 424:1042-47
171. Rost B, Riebesell U, Burkhardt S, Sültemeyer D. 2003. Carbon acquisition of bloom-forming marine phytoplankton. Limnol. Oceanogr. 48:55-67
172. Rotatore C, Colman B. 1990. Uptake of inorganic carbon by isolated chloroplasts of the unicellular green alga Chlorella ellipsoidea. Plant Physiol. 93:1597-600
173. Rotatore C, Colman B. 1991. The localization of active carbon transport at the plasma membrane in Chlorella ellipsoidea. Can. J. Bot. 69:1025-31
174. Schwarz R, Reinhold L, Kaplan A. 1995. Low activation state of ribulose-1,5-bisphosphate carboxylase/oxygenase in carboxysome-defective Synechococcus mutants. Plant Physiol. 108:183-90
175. Sherlock DJ, Raven JA. 2001. Interactions between carbon dioxide and oxygen in the photosynthesis of three species of marine red algae. Bot. J. Scotl. 53:33-43
176. Shibata M, Katoh H, Sonoda M, Ohkawa H, Shimoyama M, et al. 2002. Genes essential to sodium-dependent bicarbonate transport in cyanobacteria. Function and phylogenetic analysis. J. Biol. Chem. 277:18658-64
177. 2 uptake systems in cyanobacteria: genes involved and their phylogenetic relationship with homologous genes in other organisms. Proc. Nat. Acad. Sci. USA 98:11789-94
178. 2-uptake systems: four systems for inorganic carbon acquisition in Synechocystis sp. strain PCC6803. Funct. Plant Biol. 29:123-29
179. 2 concentration on induction of carbonic anhydrase and changes in efficiency of photosynthesis in Chlorella vulgaris 11h. Plant Cell Physiol. 26:543-59
180. Shively JM, van Keulen G, Meijer WG. 1998. Something from almost nothing: carbon dioxide fixation in chemoautotrophs. Annu. Rev. Microbiol. 52:191-230
181. Silverman DN. 2000. Marcus rate theory applied to enzymatic proton transfer. Biochim. Biophys. Acta Bioenergetics 1458:88-103
182. Smith KS, Ferry JG. 2000. Prokaryotic carbonic anhydrases. FEMS Microbiol. Revs. 24:335-66
183. So AK-C, Espie GS, Williams EB, Shively JM, Heinhorst S, Cannon GC. 2004. A novel evolutionary lineage of CAs (ε class) is a component of the carboxysome shell. J. Bacteriol. 186 : 623-30
184. 2 concentration on photosynthesis of two marine microalgae with different carbon concentrating mechanisms. Phycologia 40(Suppl.):92-93
185. 2. Proc. Natl. Acad. Sci. USA 101:7787-92
186. Spalding MH, Critchley C, Govindjee, Ogren WL. 1984. Influence of carbon dioxide concentration during growth on fluorescence induction characteristics of the green alga Chlamydomonas reinhardtii. Photosynth. Res. 5:169-76
187. Spalding MH, Van K, Wang Y, Nakamura Y. 2002. Acclimation of Chlamydomonas to changing carbon availability. Funct. Plant Biol. 29:221-30
188. Sültemeyer D. 1998. Carbonic anhydrase in eukaryotic algae: characterization, regulation and possible functions during photosynthesis. Can. J. Bot. 76:962-72
189. Sültemeyer D, Amoroso G, Fock HP. 1995. Induction of intracellular carbonic anhydrases during the adaptation to low inorganic carbon concentrations in wild-type and ca-1 mutant cells of Chlamydomonas reinhardtii. Planta 196:217-24
190. 2 and characterization of active transport. Can. J. Bot. 69:995-1002
191. - transport in cyanobacteria. Plant Physiol. 116:183-92
192. Summons RE, Jahnke LL, Hope JM, Logan GA. 1999. 2-Methylhopanoids as biomarkers for cyanobacterial oxygenic photosynthesis. Nature 400:554-57
193. +. J. Biol. Chem. 276:23450-55
194. 2. Plant Physiol. 100:2113-15
195. - uptake systems. Funct. Plant Biol. 29:251-60
196. Timmermans KR, van Leeuwe MA, de Jong JTM, McKay RML, Nolting RF, et al. 1998. Iron stress in the Pacific region of the Southern Ocean: evidence from enrichment bioassays. Mar. Ecol. Prog. Ser. 166:27-41
197. Tomitani A, Okada K, Miyashita H, Matthijs HCP, Ohno T, et al. 1999. Chlorophyll b and phycobilins in the common ancestor of cyanobacteria and chloroplasts. Nature 400:159-62
198. 2 pore with physiological functions. Nature 425:734-37
199. 2 and bicarbonate by intact cells and chloroplasts of Tetraedon minimum and Chlamydomonas noctigama. Planta 215:763-69
200. van Hunnik E, Livne A, Pogenberg V, Spijkerman E, van den Ende H, et al. 2001. Identification and localisation of a thylakoid-bound carbonic anhydrase from the green algae Tetraedon minimum (Chlorophyta) and Chlamydomonas noctigama (Chlorophyta). Planta 212:454-59
201. van Hunnik E, Sültemeyer D. 2002. A possible role for carbonic anhydrase in the lumen of chloroplast thylakoids in green algae. Funct. Plant Biol. 29:243-49
202. Van K, Spalding MH. 1999. Periplasmic carbonic anhydrase (cah1) structural gene mutant in Chlamydomonas reinhardtii. Plant Physiol. 120:757-64
203. Villarejo A, Rolland N, Martinez F, Sültemeyer DF. 2001. A new chloroplast envelope carbonic anhydrase activity is induced during acclimation to low inorganic carbon concentrations in Chlamydomonas reinhardtii. Planta 213:286-95
204. Vis ML, Entwisle TJ. 2000. Insights into the phylogeny of the Batrachospermales (Rhodophyta) with rbcl sequence data of Australian taxa. J. Phycol. 36:1175-82
205. Volokita M, Zenvirth D, Kaplan A, Reinhold L. 1984. Nature of the inorganic carbon species actively taken up by the cyanobacterium Anabaena variabilis. Plant Physiol. 76:599-602
206. Walker NA, Smith FA, Cathers IR. 1980. Bicarbonate assimilation by freshwater charophytes and higher plants. I. Membrane transport of bicarbonate is not proven. J. Membr. Biol. 57:51-58
207. Walsby AE. 1971. The pressure relationship of gas vacuoles. Proc. Royal Soc. London B. 178:301-26
208. Walsby AE. 1994. Gas vesicles. Microbiol. Rev. 58:94-144
209. Whitfield J. 2004. Geology: Time lords. Nature 429:124-25
210. Wildman RA, Hickey LJ, Dickinson MB, Berner RA, Robinson JM, et al. 2004. Burning of forest materials under late Palaeozoic oxygen levels. Geology 32:457-60
211. Xiang YB, Zhang J, Weeks DP. 2001. The cia5 gene controls formation of the carbon concentrating mechanism in Chlamydomonas. Proc. Natl. Acad. Sci. USA. 98:5341-46
212. Young EB. 1999. Interactions between photosynthetic carbon and nitrogen acquisition in the marine microalga Dunaliella tertiolecta Butcher. PhD thesis, Monash Univ., Melbourne, Australia. 228 pp.
213. 211a. Young EB, Beardall J. 2005. Modulation of photosynthesis and inorganic carbon acquisition in a marine microalga by nitrogen, iron and light availability. Can. J. Bot. In press
214. - utilization pathways. Eur. J. Phycol. 36:81-88
215. Zubkov MV, Fuchs BM, Tarran GA, Burkill PH, Amann R. 2003. High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. App. Environ. Microbiol. 69:1299-304