Large variation in the Rubisco kinetics of diatoms reveals diversity among their carbon-concentrating mechanisms

Journal of Experimental Botany

Volumn 67, Issue 11, 2016, Pages 3445-3456

  Young, Jodi N ^a,d   Heureux, Ana M C ^b   Sharwood, Robert E ^c   Rickaby, Rosalind E M ^b   Morel, François M M ^a   Whitney, Spencer M ^c  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Algae; carbon fixation; diatoms; kinetics; photosynthesis; Rubisco

Indexed keywords

CARBON; RIBULOSEBISPHOSPHATE CARBOXYLASE;

DIATOM; ENZYMOLOGY; KINETICS; METABOLISM; PHOTOSYNTHESIS; PHYTOPLANKTON;

CARBON; DIATOMS; KINETICS; PHOTOSYNTHESIS; PHYTOPLANKTON; RIBULOSE-BISPHOSPHATE CARBOXYLASE;

EID: 84973547904     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erw163     Document Type: Article

References (79)

1. Andralojc PJ, Madgwick PJ, Tao Y, et al. 2012. 2-Carboxy-d-arabinitol 1-phosphate (CA1P) phosphatase: evidence for a wider role in plant Rubisco regulation. Biochemical Journal 442, 733-742.
2. Armstrong RA, Lee C, Hedges JI, Honjo S, Wakeham SG. 2001. A new, mechanistic model for organic carbon fluxes in the ocean based on the quantitative association of POC with ballast minerals. Deep Sea Research Part II: Topical Studies in Oceanography 49, 219-236.
3. Badger MRT, Andrews J, Whitney SM, Ludwig M, Yellowlees DC, Leggat W, Price GD. 1998. The diversity and coevolution of Rubisco, plastids, pyrenoids, and chloroplast-based CO2-concentrating mechanisms in algae. Canadian Journal of Botany 76, 1052-1071.
4. Brown, JW. and Sorhannus, U. (2010) A molecular genetic timescale for the diversification of autotrophic Stramenophiles (Ochrophyta): Substantive underestimation of putative fossil ages. PLoS ONE 5(9):e12759.
5. Carmo-Silva E, Scales JC, Madgwick PJ, Parry MAJ. 2015. Optimizing Rubisco and its regulation for greater resource use efficiency. Plant, Cell and Environment 38, 1817-1832.
6. Chen X, Gao K. 2004. Photosynthetic utilisation of inorganic carbon and its regulation in the marine diatom Skeletonema costatum. Functional Plant Biology 31, 1027-1033.
7. Delwiche CF, Palmer JD. 1997. The origin of plastids and their spread via secondary symbiosis. In: Bhattacharya D, ed. The origins of algae and their plastids. Vienna: Springer-Verlag, 53-86.
8. Egan KE, Rickaby REM, Hendry KR, Halliday AN. 2013. Opening the gateways for diatoms primes Earth for Antarctic glaciation. Earth and Planetary Science Letters 375, 34-43.
9. Ehleringer JR, Cerling TE, Helliker BR. 1997. C4 photosynthesis, atmospheric CO2, and climate. Oecologia 112, 285-299.
10. Falkowski P, Schofield O, Katz M, Van de Schootbrugge B, Knoll A. 2004. Why is the land green and the ocean red? In: Thierstein H, Young J, eds. Coccolithophores. Berlin: Springer, 429-453.
11. Falkowski PG, Raven JA. 2007. Aquatic photosynthesis, Vol. 2. Princeton, NJ: Princeton University Press.
12. Furbank RT, Hatch MD. 1987. Mechanism of C4 photosynthesis: The size and composition of the inorganic carbon pool in bundle sheath cells. Plant Physiology 85, 958-964.
13. Galmes J, Kapralov MV, Andralojc PJ, Conesa MA, Keys AJ, Parry MAJ, Flexas J. 2014. Expanding knowledge of the Rubisco kinetics variability in plant species: environmental and evolutionary trends. Plant, Cell and Environment 37, 1989-2001.
14. Ghannoum O, Evans JR, Chow WS, Andrews TJ, Conroy JP, von Caemmerer S. 2005. Faster Rubisco is the key to superior nitrogenuse efficiency in NADP-malic enzyme relative to NAD-malic enzyme C(4) grasses. Plant Physiology 137, 638-650.
15. Giordano M, Beardall J, Raven JA. 2005. CO2 concentrating mechanisms in algae: mechanisms, environmental modulation, and evolution. Annual Review of Plant Biology 56, 99-131.
16. Haslam RP, Keys AJ, Andralojc PJ, Madgwick PJ, Andersson I, Grimsrud A, Eilertsen HC, Parry MAJ. 2005. Specificity of diatom Rubisco. In: Omasa K, Nouchi I, De Kok LJ, eds. Plant responses to air pollution and global change. Springer: Japan, 157-164.
17. Hauser T, Popilka L, Hartl FU, Hayer-Hartl M. 2015. Role of auxiliary proteins in Rubisco biogenesis and function. Nature Plants 1, 15065.
18. Hennon GMM, Ashowrth J, Groussman RD, Berthiaume C, Morales RL, Baliga NS, Orellana MW, Armbrust EV. 2015. Diatom acclimation to elevated CO2 via novel gene clusters and cAMP-signaling. Nature Climate Change 5, 761-765.
19. Heureux AMC, Rickaby REM. 2015. Refining our estimate of atmospheric CO2 across the Eocene-Oligocene climatic transition. Earth and Planetary Science Letters 409, 329-338.
20. Hopkinson B. 2014. A chloroplast pump model for the CO2 concentrating mechanism in the diatom Phaeodactylum tricornutum. Photosynthesis Research 121, 223-233.
21. Hopkinson BM, Dupont CL, Allen AE, Morel FMM. 2011. Efficiency of the CO2-concentrating mechanism of diatoms. Proceedings of the National Academy of Sciences, USA 108, 3830-3837.
22. 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.
23. Kane HJ, Viil J, Entsch B, Paul K, Morell MK, Andrews TJ. 1994. An improved method for measuring the CO2/O2 specificity of ribulosebisphosphate carboxylase-oxygenase. Australian Journal of Plant Physiology 21, 449-461.
24. Kane HJ, Wilkin J-M, Portis AR, John Andrews T. 1998. Potent inhibition of ribulose-bisphosphate carboxylase by an oxidized impurity in ribulose-1,5-bisphosphate. Plant Physiology 117, 1059-1069.
25. Kranz SA, Young JN, Hopkinson B, Goldman JAL, Tortell PD, Morel FMM. 2015. Low temperature reduces the energetic requirement for the CO2 concentrating mechanism in diatoms. New Phytologist 205, 192-202.
26. Kroth PG. 2015. The biodiversity of carbon assimilation. Plant Physiology 172, 76-81.
27. Laing WA, Ogren WL, Hageman RH. 1974. Regulation of soybean net photosynthetic CO2 fixation by the interaction of CO2, O2, and ribulose 1,5-diphosphate carboxylase. Plant Physiology 54, 678-685.
28. Long BM, Bahar NHA, Atkin OK. 2015. Contributions of photosynthetic and non-photosynthetic cell types to leaf respiration in Vicia faba L. and their responses to growth temperature. Plant, Cell and Environment 38, 2263-2276.
29. Long SP. 1999. Environmental responses. In: Sage RF, Monson RK, eds. C4 plant biology. Academic Press: San Diego, 215-249.
30. Losh JL, Young JN, Morel FM. 2013. Rubisco is a small fraction of total protein in marine phytoplankton. New Phytologist 198, 52-58.
31. Mueller-Cajar O, Stotz M, Bracher A. 2014. Maintaining photosynthetic CO2 fixation via protein remodelling: The Rubisco activases. Photosynthesis Research 119, 191-201.
32. Mueller-Cajar O, Whitney S. 2008. Directing the evolution of Rubisco and Rubisco activase: first impressions of a new tool for photosynthesis research. Photosynthesis Research 98, 667-675.
33. Nakajima K, Tanaka A, Matsuda Y. 2013. SLC4 family transporters in a marine diatom directly pump bicarbonate from seawater. Proceedings of the National Academy of Sciences, USA 110, 1767-1772.
34. Nelson DM, Tréguer P, Brzezinski MA, Leynaert A, Quéguiner B. 1995. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Global Biogeochemical Cycles 9, 359-372.
35. Osborne CP, Sack L. 2012. Evolution of C4 plants: A new hypothesis for an interaction of CO2 and water relations mediated by plant hydraulics. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 583-600.
36. Parry MAJ, Andralojc PJ, Scales JC, Salvucci ME, Carmo-Silva AE, Alonso H, Whitney SM. 2013. Rubisco activity and regulation as targets for crop improvement. Journal of Experimental Botany 64, 717-730.
37. Peterhansel C, Niessen M, Kebeish RM. 2008. Metabolic engineering towards the enhancement of photosynthesis. Photochemistry and Photobiology 84, 1317-1323.
38. Pierce J, Tolbert NE, Barker R. 1980. Interaction of ribulosebisphosphate carboxylase/oxygenase with transition-state analogues. Biochemistry 19, 934-942.
39. 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.
40. Price GD, Evans JR, von Caemmerer S, Yu J-W, Badger MR. 1995. Specific reduction of chloroplast glyceraldehyde-3-phosphate dehydrogenase activity by antisense RNA reduces CO2 assimilation via a reduction in ribulose bisphosphate regeneration in transgenic tobacco plants. Planta 195, 369-378.
41. Raven J, Beardall J, Giordano M. 2014. Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynthesis Research 121, 111-124.
42. Raven J, Giordano M, Beardall J, Maberly SC. 2011. Algal and aquatic plant carbon concentrating mechanisms in relation to environmental change. Photosynthesis Research 109, 1-16.
43. Raven JA. 2009 Contributions of anyoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquatic Microbial Ecology 56, 177-192.
44. Raven JA, Beardall J. 2016. The ins and outs of CO2. Journal of Experimental Botany 67, 1-13.
45. 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.
46. Read BA, Tabita FR. 1994. High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial rubisco containing 'algal' residue modifications. Archives of Biochemistry and Biophysics 312, 210-218.
47. Reinfelder JR. 2010. Carbon concentrating mechanisms in eukaryotic marine phytoplankton. Annual Review of Marine Science 3, 291-315.
48. Reinfelder JR, Kraepiel AM, Morel FM. 2000. Unicellular C4 photosynthesis in a marine diatom. Nature 407, 996-999.
49. Reinfelder JR, Milligan AJ, Morel FMM. 2004. The role of the C4 pathway in carbon accumulation and fixation in a marine diatom. Plant Physiology 135, 2106-2111.
50. Rigobello-Masini M, Penteado JCP, Tiba M, Masini JC. 2012. Study of photorespiration in marine microalgae through the determination of glycolic acid using hydrophilic interaction liquid chromatography. Journal of Separation Science 35, 20-28.
51. Roberts K, Granum E, Leegood RC, Raven JA. 2007. Carbon acquisition by diatoms. Photosynthesis Research 93, 79-88.
52. Rost B, Riebesell U, Burkhardt S, Sültemeyer D. 2003. Carbon acquisition of bloom-forming marine phytoplankton. Limnology and Oceanography 48, 55-67.
53. Sage RF. 2001. Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biology 3, 202-213.
54. Sage RF. 2004. Tansley review: The evolution of C4 photosynthesis. New Phytologist 161, 341-371.
55. Savir Y, Noor E, Milo R, Tlusty T. 2010. Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape. Proceedings of the National Academy of Sciences, USA 107, 3475-3480.
56. Schnitzler Parker M, Armbrust E, Piovia-Scott J, Keil RG. 2004. Induction of photorespiration by light in the centric diatom Thalassiosisra weissflogii (Bacillariophyceae): molecular characterization and physiological consequences. Journal of Phycology 40, 557-567.
57. Seemann JR, Badger MR, Berry JA. 1984. Variations in the specific activity of ribulose-1,5-bisphosphate carboxylase between species utilizing differing photosynthetic pathways. Plant Physiology 74, 791-795.
58. Sharwood RE, von Caemmerer S, Maliga P, Whitney SM. 2008. The catalytic properties of hybrid rubisco comprising tobacco small and sunflower large subunits mirror the kinetically equivalent source rubiscos and can support tobacco growth. Plant Physiology 146, 83-96.
59. Sunda WG, Price NM, Morel FMM. 2005. Trace metal ion buffers and their use in culture studies. In: Andersen RA, ed. Algal culturing techniques. Amsterdam: Elsevier, 35-63.
60. Tabita FR, Satagopan S, Hanson TE, Kreel NE, Scott SS. 2008. Distinct form I, II, III, and IV Rubisco proteins from the three kingdoms of life provide clues about Rubisco evolution and structure/function relationships. Journal of Experimental Botany 59, 1515-1524.
61. Tcherkez G. 2013. Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/oxygenase and consequences for kinetic parameters. Plant, Cell and Environment 36, 1586-1596.
62. Tcherkez G. 2015. The mechanism of Rubisco-catalyzed oxygenation. Plant, Cell and Environment 39 (5), 983-997.
63. Tcherkez GGB, Farquhar GD, Andrews TJ. 2006. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. Proceedings of the National Academy of Sciences, USA 103, 7246-7251.
64. Tortell PD, Rau GH, Morel FM. 2000. Inorganic carbon acquisition in coastal Pacific phytoplankton communities. Limnology and Oceanography 45, 1485-1500.
65. Tsai YC, Lapina MC, Bhushan S, Mueller-Cajar O. 2016. Identification and characterization of multiple rubisco activases in chemoautotrophic bacteria. Nature Communications. 6, 8883.
66. von Caemmerer S, Furbank R. 2003. The C4 pathway: an efficient CO2 pump. Photosynthesis Research 77, 191-207.
67. Way DA, Katul GG, Manzoni S, Vico G. 2014. Increasing water use efficiency along the C3 to C4 evolutionary pathway: A stomatal optimization perspective. Journal of Experimental Botany 65, 3683-3693.
68. Whitehead L, Long BM, Price GD, Badger MR. 2014. Comparing the in vivo function of α-carboxysomes and β-carboxysomes in two model cyanobacteria. Plant Physiology 165, 398-411.
69. Whitney SM, Baldet P, Hudson GS, Andrews TJ. 2001. Form I Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. The Plant Journal 26, 535-547.
70. Whitney SM, Houtz RL, Alonso H. 2011. Advancing our understanding and capacity to engineer nature's CO2-sequestering enzyme, Rubisco. Plant Physiology 155, 27-35.
71. Whitney SM, Sharwood RE. 2007. Linked Rubisco subunits can assemble into functional oligomers without impeding catalytic performance. Journal of Biological Chemistry 282, 3809-3818.
72. Whitney SM, von Caemmerer S, Hudson GS, Andrews TJ. 1999. Directed mutation of the Rubisco large subunit of tobacco influences photorespiration and growth. Plant Physiology 121, 579-588.
73. Yeoh H-H, Badger MR, Watson L. 1980. Variations in Km(CO2) of ribulose-1,5-bisphosphate carboxylase among grasses. Plant Physiology 66, 1110-1112.
74. Yoon HS, Hackett JD, Pinto G, Bhattacharya D. 2002. The single, ancient origin of chromist plastids. Proceedings of the National Academy of Sciences, USA 99, 15507-15512.
75. Young JN, Bruggeman J, Rickaby REM, Erez J, Conte M. 2013. Evidence for changes in carbon isotopic fractionation by phytoplankton between 1960 and 2010. Global Biogeochemical Cycles 27, 505-515.
76. Young JN, Kranz SA, Goldman JAL, Tortell PD, Morel FM. 2015. Antarctic phytoplankton down-regulate their carbon concentrating mechanisms under high CO2 with no change in growth rates. Marine Ecology Progress Series 532, 13-28.
77. Young JN, Rickaby REM, Kapralov MV, Filatov DA. 2012. Adaptive signals in algal Rubisco reveal a hisotry of ancient atmospheric CO2. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 483-492.
78. Zelitch I, Schultes NP, Peterson RB, Brown P, Brutnell TP. 2009. High glycolate oxidase activity is required for survival of maize in normal air. Plant Physiology 149, 195-204.
79. Zhu G, Jensen RG. 1991. Xyulose 1,5-bisphosphate synthesized by ribulose 1,5-bisphosphate carboxylase/oxygenase during catalysis binds to decarbamylated enzyme. Plant Physiology 97, 1348-1353.