The evolution of inorganic carbon concentrating mechanisms in photosynthesis

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 363, Issue 1504, 2008, Pages 2641-2650

  Raven, John A ^a   Cockell, Charles S ^b   De La Rocha, Christina L ^c  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b OPEN UNIVERSITY   (United Kingdom)

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

Author keywords

Alga; C4 photosynthesis; Crassulacean acid metabolism; Cyanobacteria; Embryophytes; Stromatolites

Indexed keywords

BIOCHEMISTRY; CARBON DIOXIDE; CYANOBACTERIUM; EVOLUTION; INORGANIC CARBON; IRON; NITROGEN; OXYGEN; OZONE; PHOSPHORUS; PHOTOSYNTHESIS; PHOTOSYNTHETICALLY ACTIVE RADIATION; STROMATOLITE; VASCULAR PLANT;

ALGAE; CRASSULACEAE; CYANOBACTERIA; EMBRYOPHYTA; TRACHEOPHYTA;

EID: 47249139878     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2008.0020     Document Type: Conference Paper

References (87)

1. Anbar, A. D. et al. 2007 A whiff of oxygen before the Great Oxidation Event? Science 317, 1903-1906. (doi:10.1126/science. 1140325)
2. 2-concentrating mechanisms in algae. Can. J. Bot. 76, 1052-1071. (doi:10.1139/cjb-76-6-1052)
3. 2-concentrating mechanisms in cyanobacteria. Funct. Plant Biol. 29, 161-173. (doi:10.1071/PP01213)
4. Batchellor, M. T., Burne, R. V., Henry, B. I. & Jackson, M. J. 2004 A case for biotic morphogenesis of coniform stromatolites. Phys. A: Stat. Theor. Phys. 337, 319-326. (doi:10.1016/j.physa.2004.01.065)
5. Beardall, J., Mukerji, D., Glover, H. E. & Morris, I. 1976 The path of carbon in photosynthesis by marine phytoplankton. J. Phycol. 12, 409-417.
6. Beardall, J., Heraud, P., Roberts, S., Shelly, K. & Stojkovic, S. 2002 Effects of UV-B radiation on inorganic carbon acquisition by the marine microalga Dunaliella tertiolecta (Chlorophyceae). Phycologia 41, 268-272.
7. Beer, S., Bjork, M., Hellblom, F. & Avelsson, L. 2002 Inorganic carbon utilization in marine angiosperms (seagrasses). Funct. Plant Biol. 29, 349-354. (doi:10.1071/PP01185)
8. Berg, I. A., Koskelkorn, D., Buckell, W. & Fuchs, G. 2007 A 3-hydroxypropionate/4-hydroxybutyrate autotrophic carbon dioxide assimilation pathway in Archaea. Science 318, 1782-1786. (doi:10.1126/science. 1149976)
9. 2 over Phanerozoic time. Am. J. Sci. 301, 182-204. (doi:10.2475/ajs.301.2.182)
10. 4 plants. Carnegie Inst. Wash. Yearbook 1992-1993, 60-64.
11. Brocks, J. J. & Pearson, A. 2005 Building the biomarker tree of life. Rev. Miner. Geochem. Mol. Geomicrobiol. 59, 233-258. (doi:10.2138/rmg.2005.59.10)
12. 2] by an inorganic carbon-concentrating mechanism in Cyanophora paradoxa. Plant Cell Environ. 30, 1422-1435. (doi:10.1111/j.1365-3040.2007.01715.x)
13. Burns, T. A., MacKenzie, T. D. B. & Campbell, D. A. 2006 Inorganic carbon repletion constrains light acclimation in the cyanobacterium Synechococcus elongatus. J. Phycol. 42, 610-621. (doi:10.1111/j.1529-8817.2006.00220.x)
14. Caldeira, K. & Kasting, J. F. 1992 The life span of the biosphere revisited. Nature 360, 721-723. (doi:10.1038/360721a0)
15. 2 concentrations during the Palaeozoic era. Nature 449, 198-201. (doi:10.1038/nature06085)
16. Colman, B., Huertas, I. E., Bhatti, S. & Dason, J. S. 2002 The diversity of inorganic carbon concentrating mechanisms in eukaryotic microalgae. Funct. Plant Biol. 29, 261-270. (doi:10.1071/PP01184)
17. Correia, C. M., Pereira, J. M. M., Coutinho, J. F., Björn, L. O. & Torres-Pereira, J. M. G. 2005 Ultraviolet-B radiation and nitrogen affect the photosynthesis of maize: a Mediterranean field study. Eur. J. Agron. 22, 337-347. (doi:10.1016/j.eja.2004.05.002)
18. Decker, J. E. & de Wit, M. J. 2006 Carbon isotope discrimination evidence for CAM photosynthesis in the Mesozoic. Terra Nova 18, 9-17. (doi:10.1111/j.1365-3121.2005.00654.x)
19. 4 photosynthesis versus the dual-cell (Kranz) paradigm. Annu. Rev. Plant Biol. 55, 173-196. (doi:10.1146/annurev.arplant. 55.031903.141725)
20. 2 and climate. Oecologia 112, 285-299. (doi:10.1007/s004420050311)
21. Finkel, Z. V., Katz, M. E., Wright, J. D., Schofield, O. M. E. & Falkowski, P. G. 2005 Climatically driven macroevolutionary patterns in the size of marine diatoms over the Cenozoic. Proc. Natl Acad. Sci. USA 102, 8927-8932. (doi:10.1073/pnas.0409907102)
22. Finkel, Z. V., Quigg, A., Raven, J. A., Reinfelder, J. R., Schofield, O. E. & Falkowski, P. G. 2006 Irradiance and elemental stoichiometry of marine phytoplankton. Limnol. Oceanogr. 51, 2690-2701.
23. Franck, S., Bounama, C. & von Bloh, W. 2006 Causes and timing of future biosphere extinctions. Biogeosciences 3, 85-92.
24. 2 fixation in marine phytoplankton: a double-edged sword. Plant Physiol. 144, 54-59. (doi:10.1104/pp.107.098491)
25. 2 concentrating mechanisms in algae mechanisms: environmental-modulation, andevolution. Annu. Rev. Plant Biol. 56, 99-131. (doi:10.1146/annurev.arplant.56.032604.144052)
26. Griffiths, H., Cousins, A. B., Badger, M. R. & von Caemmerer, S. 2007 Discrimination in the dark. Resolving the interplay between metabolic and physical constraints to phosphoenolpyruvate carboxylase activity during the crassulacean acid metabolism cycle. Plant Physiol. 143, 1055-1067. (doi:10.1104/pp.106.088302)
27. Harland, W. B. 2007 Origins and assessment of Snowball Earth hypotheses. Geol. Mag. 144, 633-642. (doi:10.1017/S0016756807003391)
28. - dehydration maintained by acid zones in the plasma membrane in an important component of the photosynthetic carbon uptake in Ruppia cirrhosa. Photosynth. Res. 77, 173-181. (doi:10.1023/A:1025809415048)
29. Iglesias-Rodriguez, M. D., Nimer, N. A. & Merrett, M. J. 1998 Carbon dioixide concentrating mechanism and the development of extracellular carbonic anhydrase in the marine picoeukaryote Micromonas pusilla. New Phytol. 140, 685-690. (doi:10.1046/j.1469-8137.1998.00309.x)
30. 2 regulation in Chlamydomonas reinhardtii using genome-wide approaches. Photosynth. Res. 75, 111-125. (doi:10.1023/A:1022800630430)
31. Johnson, G. A. & Day, T. A. 2002 Enhancement of photosynthesis by Sorghum bicolor by ultraviolet radiation. Physiol. Plant 116, 554-562. (doi:10.1034/j.1399-3054.2002.1160415.x)
32. Katz, M. E., Wright, J. D., Miller, G. D., Cramer, B. S., Fennel, K. & Falkowski, P. G. 2005 Biological overprint of the geological carbon cycle. Mar. Geol. 217, 323-338. (doi:10.1016/j.margeo.2004.08.005)
33. Kaufman, A. J. et al. 2007 Late Archean biospheric oxygenation and atmospheric evolution. Science 317, 1900-1903. (doi:10.1126/science.1138700)
34. Keeley, J. E. 1998 CAM photosynthesis in submerged aquatic plants. Bot. Rev. 64, 121-175. (doi:10.1007/BF02856581)
35. 4 carbon-concentrating mechanisms. Int. J. Plant Sci. 8, 683-690.
36. 4 grasslands. Ecol. Lett. 8, 683-690. (doi:10.1111/j.1461-0248.2005.00767.x)
37. Kevekordes, K. et al. 2006 Inorganic carbon acquisition by eight species of Caulerpa (Caulerpaceae, Chlorophyta). Phycologia 45, 442-449. (doi:10.2216/05-55.1.)
38. Konhauser, K. O., Lalondew, S. V., Amskold, L. & Holland, H. D. 2007 Was there an Archean phosphate crisis? Science 315, 1124. (doi:10.1126/science.1136328)
39. Korb, R. E., Raven, J. A., Johnston, A. M. & Leftley, J. W. 1996 Effects of cell size and growth rate in stable isotope discrimination by two species of marine diatom. Mar. Ecol. Prog. Ser. 143, 283-288. (doi:10.3354/meps143283)
40. Lezcano, I., Pérez-Rey, R., Baluja, C. & Sánchez, E. 1999 Ozone inactivation of Pseudomonas aeruginosa, Escherichia coli, Shigella sonnei and Salmonella typhimurum in water. Ozone Sci. Eng. 21, 293-300. (doi:10.1080/01919519908547242)
41. Lezcano, I., Pérez-Rey, R., Gutiérrez, M. S., Baluja, C. & Sánchez, E. 2000 Ozone inactivation of microorganisms in water. Gram positive bacteria and yeast. Ozone Sci. Eng. 23, 183-187. (doi:10.1080/01919510108962001)
42. Lovelock, J. E. & Whitfield, M. 1982 Life-span of the biosphere. Nature 296, 561-663. (doi:10.1038/296561a0)
43. Maberly, S. C. & Madsen, T. V. 2002 Freshwater angiosperm carbon concentrating mechanisms: processes and patterns. Funct. Plant Biol. 29, 393-405. (doi:10.1071/PP01187)
44. MacKenzie, T. D. B., Burns, R. A. & Campbell, D. A. 2002 Carbon status constrains light acclimation in the cyanobacterium Synechococcus elongatus. Plant Physiol. 136, 3301-3312. (doi:10.1104/pp.104.047936)
45. 4 pathway of marine diatoms. Plant Physiol. 146, 300-309. (doi:10.1104/pp.107.110569)
46. Moore, G., Griffith, C. & Peters, A. 2000 Bactericidal properties of ozone and its potential application as a terminal disinfectant. J. Food Protect. 63, 1100-1106.
47. Moroney, J. V. & Ynalvez, R. A. 2007 A proposed carbon dioxide concentrating mechanism in Chlamydomonas reinhardti. Eukaryot. Cell 6, 1251-1259. (doi:10.1128/EC.00064-07)
48. 4 plants. Phil. Trans. R. Soc. B 361, 173-194. (doi:10.1098/rstb.2005.1737)
49. 2 concentrating mechanisms in cyanobacteria: their diversity and evolution. J. Exp. Bot. 77, 83-94.
50. 2-concentrating mechanism (CCM): functional components, Ci transporters, diversity, genetic regulation and prospects for engineering into plants. J. Exp. Bot. (doi:10.1093/jxb/erm112)
51. 2 in the chloroplast of microalgae. Sov. Plant Physiol. 39, 470-476.
52. Rampino, M. R. & Caldeira, K. 1994 The Goldilocks problem - climatic evolution and long-term habitability of the terrestrial planets. Annu. Rev. Astron. Astrophys. 32, 83-114. (doi:10.1146/annurev.aa.32.090194. 000503)
53. Raven, J. A. 1980 Nutrient uptake by microalgae. Adv. Microbial. Physiol. 21, 47-226.
54. Raven, J. A. 1990 Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and C assimilation pathway. New Phytol. 116, 1-18. (doi:10.1111/j.1469- 8137.1990.tb00505.x)
55. 2 and temperature. Plant Cell Environ. 14, 779-794. (doi:10.1111/j.1365-3040.1991.tb01442.x)
56. Raven, J. A. 1991b Implications of inorganic carbon utilization - ecology, evolution and geochemistry. Can. J. Bot. 69, 908-924. (doi:10.1139/b91-118)
57. 2 concentrating mechanisms: a role for thylakoid lumen acidification. Plant Cell Eviron. 24, 261-265. (doi:10.1111/j.1365-3040.2001.00662.x)
58. Raven, J. A. 1997b The role of marine biota in the evolution of terrestrial biota: gases and genes. Biogeochemistry 39, 139-164. (doi:10.1023/A:1005855528289)
59. Raven, J. A. 2003 Inorganic carbon concentrating mechanisms in relation to the biology of algae. Photosynth. Res. 77, 155-171. (doi:10.1023/A:1025877902752)
60. Raven, J. A. & Larkum, A. W. D. 2007 Are there ecological implications for the proposed energetic restrictions on photosynthetic oxygen evolution at high oxygen concentrations. Photosynth. Res. 94, 31-42. (doi:10.1007/s11120-007-9211-z)
61. Raven, J. A. et al. 2002a Mechanistic interpretation of carbon isotope discrimination by marine macroalgae and sea-grasses. Funct. Plant Biol. 29, 355-378. (doi:10.1071/PP01201)
62. Raven, J. A. et al. 2002b Seaweeds in cold seas: evaluation and carbon acquisition. Ann. Bot. 90, 525-536. (doi:10.1093/aob/mcf171)
63. Raven, J. A., Andrews, M. & Quigg, A. 2005a The evolution of oligotrophy: implications for the breeding of crop plants for low input agricultural systems. Ann. Appl. Biol. 146, 261-280. (doi:10.1111/j.1744-7348.2005.040138.x)
64. 2 concentrating mechanisms. Can. J. Bot. 83, 879-890. (doi:10.1139/b05-074)
65. Raven, J. A., Brown, K., Mackay, M., Beardall, J., Giordano, M., Granum, E., Leegood, R. C., Kilminster, K. & Walker, D. I. 2005c Iron, nitrogen, phosphorus and zinc cycling and consequences for primary productivity in the oceans. In SGM symposium 65: micro-organisms and Earth systems-advances in geomicrobiology (eds G. M. Gadd, K. T. Semple & H. M. Lappin-Scott), pp. 247-272. Cambridge, UK: Cambridge University Press.
66. Raven, J. A., Giordano, M. & Beardall, J. 2008 Insights into the evolution of CCMs from comparison with other resource acquisition and assimilation processes. Physiol. Plant 133, 4-14. (doi:10.1111/j.1399-3054.2007.01024.x)
67. 4 photosynthesis in diatoms. Nature 407, 996-999. (doi:10.1038/35039612)
68. Reiskind, J. B., Seaman, P. T. & Bowes, G. 1988 Alternative methods of photosynthetic carbon assimilation in marine macroalgae. Plant Physiol. 87, 686-692.
69. Riding, R. 2006 Cyanobacterial calcification, carbon dioxide concentrating mechanisms, and Proterozoic-Cambrian changes in atmospheric composition. Geobiology 4, 299-316. (doi:10.1111/j.1472-4669.2006. 00087.x)
70. Roberts, K., Granum, E., Leegood, R. C. & Raven, J. A. 2007a Carbon metabolism in diatoms. Photosynth. Res. 93, 79-88. (doi:10.1007/s11120-007-9172-2)
71. 4 pathways of carbon assimilation in marine diatoms is under genetic, not environmental, control. Plant Physiol. 145, 230-235. (doi:10.1104/pp.107.102616)
72. Rosen, R. 1967 Optimality principles in biology. London, UK: Butterworths.
73. 2 concentrations over the past 420 million years. Nature 446, 530-532. (doi:10.1038/nature05699)
74. 4 plant biology. San Diego, CA: Academic Press.
75. 4 photosynthesis incompatible? Funct. Plant Biol. 29, 775-785. (doi:10.1071/PP01217)
76. 2 levels. Precambrian Res. 147, 148-155. (doi:10.1016/j.precamres. 2006.02.004)
77. Smith, E. C. & Griffiths, H. 1996 A pyrenoid-based carbon-concentrating mechanism is present in terrestrial bryophytes of the class Anthocerotae. Planta 200, 203-212.
78. Sobrino, C., Neal, P. J. & Lubian, L. M. 2004 Interaction of UV radiation and inorganic carbon supply in the inhibition of photosynthesis: spectral and temporal responses of two marine phytoplankton. Photochem. Photobiol. 81, 384-393. (doi:10.1562/2004-08-27-RA-295.1)
79. Spalding, M. H. 2007 Microalgal carbon dioxide-concentrating mechanisms:Chlamydomonas inorganic carbon transporters. J. Exp. Bot. (doi:10.1093/jxb/erm128)
80. 2 in suspensions of carbonic anhydrase-loaded plasma-membrane vesicles. Planta 200, 358-368. (doi:10.1007/BF00200304)
81. Tabita, F. R., Hanson, T. E., Satagopan, S., Witte, B. H. & Kreel, N. E. 2008 Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Phil. Trans. R. Soc. B 363, 2629-2640. (doi:10.1098/rstb. 2008.0023)
82. Tcherkez, G. G. B., Farquhar, G. D. & Andrews, T. J. 2006 Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimised. Proc. Natl Acad. Sci. USA 103, 7246-7251. (doi:10.1073/pnas.0600605103)
83. Uku, J., Beer, S. & Bjork, M. 2005 Buffer sensitivity of photosynthetic carbon utilization in eight tropical seagrasses. Mar. Biol. 147, 1085-1090. (doi:10.1007/s00227-005-0019-0)
84. 2 regulates multiple acclimation states. Can. J. Bot. 83, 796-809. (doi:10.1139/b05-064)
85. Vovides, A. P., Etherington, J. R., Dresser, P. Q., Groenhof, A., Iglesias, C. & Ramirez, J. F. 2002 CAM-cycling in the cycad Dioon edule Lindl. in its natural tropical deciduous forest habitat in central Veracruz, Mexico. Bot. J. Linn. Soc. 138, 155-162. (doi:10.1046/j.1095-8339.2002.138002155.x)
86. Walker, N. A., Smith, F. A. & Cathers, I. R. 1980 Bicarbonate assimilation by fresh-water charophytes and higher plants. I. Membrane transport of bicarbonate is not proven. J. Membr. Biol. 57, 51-58. (doi:10.1007/BF01868985)
87. Winter, K. & Smith, J. A. C. (eds) 1995 Crassulacean acid metabolism: biochemistry, ecophysiology and evolution. Berlin, Germany: Springer.