1932

Abstract

Carbon fixation is the process by which CO is converted from a gas into biomass. The Calvin–Benson–Bassham cycle (CBB) is the dominant carbon-consuming pathway on Earth, driving >99.5% of the ∼120 billion tons of carbon that are converted to sugar by plants, algae, and cyanobacteria. The carboxylase enzyme in the CBB, ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco), fixes one CO molecule per turn of the cycle into bioavailable sugars. Despite being critical to the assimilation of carbon, rubisco's kinetic rate is not very fast, limiting flux through the pathway. This bottleneck presents a paradox: Why has rubisco not evolved to be a better catalyst? Many hypothesize that the catalytic mechanism of rubisco is subject to one or more trade-offs and that rubisco variants have been optimized for their native physiological environment. Here, we review the evolution and biochemistry of rubisco through the lens of structure and mechanism in order to understand what trade-offs limit its improvement. We also review the many attempts to improve rubisco itself and thereby promote plant growth.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biochem-040320-101244
2023-06-20
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/biochem/92/1/annurev-biochem-040320-101244.html?itemId=/content/journals/10.1146/annurev-biochem-040320-101244&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Raven JA. 2009. Contributions of anoxygenic and oxygenic phototrophy and chemolithotrophy to carbon and oxygen fluxes in aquatic environments. Aquat. Microb. Ecol. 56:177–92
    [Google Scholar]
  2. 2.
    Bar-On YM, Milo R 2019. The global mass and average rate of rubisco. PNAS 116:104738–43
    [Google Scholar]
  3. 3.
    Andersson I. 1996. Large structures at high resolution: the 1.6 Å crystal structure of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase complexed with 2-carboxyarabinitol bisphosphate. J. Mol. Biol. 259:160–74
    [Google Scholar]
  4. 4.
    Lundqvist T, Schneider G. 1991. Crystal structure of the ternary complex of ribulose-1,5-bisphosphate carboxylase, Mg(II) and activator CO2 at 2.3-Å resolution. Biochemistry 30:904–8
    [Google Scholar]
  5. 5.
    Fischer WW, Hemp J, Johnson JE. 2016. Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44:647–83
    [Google Scholar]
  6. 6.
    Tcherkez GGB, Farquhar GD, Andrews TJ. 2006. Despite slow catalysis and confused substrate specificity, all ribulose bisphosphate carboxylases may be nearly perfectly optimized. PNAS 103:7246–51
    [Google Scholar]
  7. 7.
    Savir Y, Noor E, Milo R, Tlusty T. 2010. Cross-species analysis traces adaptation of Rubisco toward optimality in a low-dimensional landscape. PNAS 107:3475–80
    [Google Scholar]
  8. 8.
    Morell MK, Paul K, Kane HJ, Andrews TJ. 1992. Rubisco: maladapted or misunderstood. Aust. J. Bot. 40:431–41
    [Google Scholar]
  9. 9.
    Bar-Even A, Noor E, Savir Y, Liebermeister W, Davidi D et al. 2011. The moderately efficient enzyme: evolutionary and physicochemical trends shaping enzyme parameters. Biochemistry 50:4402–10
    [Google Scholar]
  10. 10.
    Bathellier C, Tcherkez G, Lorimer GH, Farquhar GD. 2018. Rubisco is not really so bad. Plant Cell Environ 41:705–16
    [Google Scholar]
  11. 11.
    Zhan C-G, Niu S, Ornstein RL. 2001. Theoretical studies of nonenzymatic reaction pathways for the three reaction stages of the carboxylation of ribulose-1,5-bisphosphate. J. Chem. Soc. Perkin Trans. 2 2001.23–29
    [Google Scholar]
  12. 12.
    Farquhar GD. 1979. Models describing the kinetics of ribulose biphosphate carboxylase-oxygenase. Arch. Biochem. Biophys. 193:456–68
    [Google Scholar]
  13. 13.
    Cleland WW, Andrews TJ, Gutteridge S, Hartman FC, Lorimer GH. 1998. Mechanism of rubisco: the carbamate as general base. Chem. Rev. 98:549–62
    [Google Scholar]
  14. 14.
    Bathellier C, Yu L-J, Farquhar GD, Coote ML, Lorimer GH, Tcherkez G. 2020. Ribulose 1,5-bisphosphate carboxylase/oxygenase activates O2 by electron transfer. PNAS 117:24234–42
    [Google Scholar]
  15. 15.
    Tawfik DS. 2014. Accuracy-rate tradeoffs: How do enzymes meet demands of selectivity and catalytic efficiency?. Curr. Opin. Chem. Biol. 21:73–80
    [Google Scholar]
  16. 16.
    Bar-Even A, Salah Tawfik D 2013. Engineering specialized metabolic pathways—is there a room for enzyme improvements?. Curr. Opin. Biotechnol. 24:310–19
    [Google Scholar]
  17. 17.
    Arnold FH. 2018. Directed evolution: bringing new chemistry to life. Angew. Chem. Int. Ed. Engl. 57:4143–48
    [Google Scholar]
  18. 18.
    Flamholz AI, Prywes N, Moran U, Davidi D, Bar-On YM et al. 2019. Revisiting trade-offs between rubisco kinetic parameters. Biochemistry 58:3365–76
    [Google Scholar]
  19. 19.
    Gutteridge S, Lorimer G, Pierce J. 1988. Details of the reactions catalysed by mutant forms of rubisco. Plant Physiol. Biochem. 26:675–82
    [Google Scholar]
  20. 20.
    Gutteridge S, Sigal I, Thomas B, Arentzen R, Cordova A, Lorimer G. 1984. A site-specific mutation within the active site of ribulose-1,5-bisphosphate carboxylase of Rhodospirillum rubrum. EMBO J 3:2737–43
    [Google Scholar]
  21. 21.
    Cai Z, Liu G, Zhang J, Li Y. 2014. Development of an activity-directed selection system enabled significant improvement of the carboxylation efficiency of Rubisco. Protein Cell 5:552–62
    [Google Scholar]
  22. 22.
    Amichay D, Levitz R, Gurevitz M. 1993. Construction of a Synechocystic PCC6803 mutant suitable for the study of variant hexadecameric ribulose bisphosphate carboxylase/oxygenase enzymes. Plant Mol. Biol. 23:465–76
    [Google Scholar]
  23. 23.
    Mueller-Cajar O, Whitney SM. 2008. Directing the evolution of Rubisco and Rubisco activase: first impressions of a new tool for photosynthesis research. Photosynth Res 98:667–75
    [Google Scholar]
  24. 24.
    Wilson RH, Alonso H, Whitney SM. 2016. Evolving Methanococcoides burtonii archaeal Rubisco for improved photosynthesis and plant growth. Sci. Rep. 6:22284
    [Google Scholar]
  25. 25.
    Durão P, Aigner H, Nagy P, Mueller-Cajar O, Hartl FU, Hayer-Hartl M. 2015. Opposing effects of folding and assembly chaperones on evolvability of Rubisco. Nat. Chem. Biol. 11:148–55
    [Google Scholar]
  26. 26.
    Satagopan S, Huening KA, Tabita FR. 2019. Selection of cyanobacterial (Synechococcus sp. strain PCC 6301) RubisCO variants with improved functional properties that confer enhanced CO2-dependent growth of Rhodobacter capsulatus, a photosynthetic bacterium. MBio 10:4e01537-19
    [Google Scholar]
  27. 27.
    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. J. Exp. Bot. 59:1515–24
    [Google Scholar]
  28. 28.
    Davidi D, Shamshoum M, Guo Z, Bar-On YM, Prywes N et al. 2020. Highly active rubiscos discovered by systematic interrogation of natural sequence diversity. EMBO J 39:e104081
    [Google Scholar]
  29. 29.
    Farquhar GD, von Caemmerer S, Berry JA. 1980. A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90
    [Google Scholar]
  30. 30.
    Wu A, Brider J, Busch FA, Chen M, Chenu K et al. 2022. A cross-scale analysis to understand and quantify effects of photosynthetic enhancement on crop growth and yield. bioRxiv 2022.07.06.498957. http://doi.org/10.1101/2022.07.06.498957
    [Crossref]
  31. 31.
    Busch FA, Sage RF, Farquhar GD. 2018. Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nat. Plants 4:46–54
    [Google Scholar]
  32. 32.
    Bloom AJ, Lancaster KM. 2018. Manganese binding to Rubisco could drive a photorespiratory pathway that increases the energy efficiency of photosynthesis. Nat. Plants 4:414–22
    [Google Scholar]
  33. 33.
    Sinclair TR, Rufty TW, Lewis RS. 2019. Increasing photosynthesis: unlikely solution for world food problem. Trends Plant Sci 24:111032–39
    [Google Scholar]
  34. 34.
    Raines CA. 2003. The Calvin cycle revisited. Photosynth. Res. 75:1–10
    [Google Scholar]
  35. 35.
    Iñiguez C, Aguiló-Nicolau P, Galmés J. 2021. Improving photosynthesis through the enhancement of Rubisco carboxylation capacity. Biochem. Soc. Trans. 49:2007–19
    [Google Scholar]
  36. 36.
    Zhu X-G, Portis AR Jr., Long SP. 2004. Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27:155–65
    [Google Scholar]
  37. 37.
    Iqbal WA, Miller IG, Moore RL, Hope IJ, Cowan-Turner D, Kapralov MV. 2021. Rubisco substitutions predicted to enhance crop performance through carbon uptake modelling. J. Exp. Bot. 72:6066–75
    [Google Scholar]
  38. 38.
    Singh AK, Santos-Merino M, Sakkos JK, Walker BJ, Ducat DC. 2022. Rubisco regulation in response to altered carbon status in the cyanobacterium Synechococcus elongatus PCC 7942. Plant Physiol 189:2874–88
    [Google Scholar]
  39. 39.
    Kawashima N, Wildman SG. 1971. Studies on fraction-I protein. I. Effect of crystallization of fraction-I protein from tobacco leaves on ribulose diphosphate carboxylase activity. Biochim. Biophys. Acta Protein Struct. 229:240–49
    [Google Scholar]
  40. 40.
    Wildman SG. 2002. Along the trail from Fraction I protein to Rubisco (ribulose bisphosphate carboxylase-oxygenase). Photosynth. Res. 73:243–50
    [Google Scholar]
  41. 41.
    Dorner RW, Kahn A, Wildman SG. 1957. The proteins of green leaves. VII. Synthesis and decay of the cytoplasmic proteins during the life of the tobacco leaf. J. Biol. Chem. 229:945–52
    [Google Scholar]
  42. 42.
    Quayle JR, Fuller RC, Benson AA, Calvin M. 1954. Enzymatic carboxylation of ribulose diphosphate. J. Am. Chem. Soc. 76:3610–11
    [Google Scholar]
  43. 43.
    Bassham JA, Benson AA, Kay LD, Harris AZ, Wilson AT, Calvin M. 1954. The path of carbon in photosynthesis. XXI. The cyclic regeneration of carbon dioxide acceptor. J. Am. Chem. Soc. 76:1760–70
    [Google Scholar]
  44. 44.
    Weissbach A, Horecker BL, Hurwitz J. 1956. The enzymatic formation of phosphoglyceric acid from ribulose diphosphate and carbon dioxide. J. Biol. Chem. 218:795–810
    [Google Scholar]
  45. 45.
    Anderson LE, Price GB, Fuller RC. 1968. Molecular diversity of the ribulose-1,5-diphosphate carboxylase from photosynthetic microorganisms. Science 161:482–84
    [Google Scholar]
  46. 46.
    Bowes G, Ogren WL, Hageman RH. 1971. Phosphoglycolate production catalyzed by ribulose diphosphate carboxylase. Biochem. Biophys. Res. Commun. 45:716–22
    [Google Scholar]
  47. 47.
    Lorimer GH, Andrews TJ, Tolbert NE. 1973. Ribulose diphosphate oxygenase. II. Further proof of reaction products and mechanism of action. Biochemistry 12:18–23
    [Google Scholar]
  48. 48.
    Lorimer GH, Miziorko HM. 1980. Carbamate formation on the ε-amino group of a lysyl residue as the basis for the activation of ribulosebisphosphate carboxylase by CO2 and Mg2+. Biochemistry 19:5321–28
    [Google Scholar]
  49. 49.
    Lorimer GH. 1981. Ribulosebisphosphate carboxylase: amino acid sequence of a peptide bearing the activator carbon dioxide. Biochemistry 20:1236–40
    [Google Scholar]
  50. 50.
    Lorimer GH, Badger MR, Andrews TJ. 1976. The activation of ribulose-1,5-bisphosphate carboxylase by carbon dioxide and magnesium ions. Equilibria, kinetics, a suggested mechanism, and physiological implications. Biochemistry 15:529–36
    [Google Scholar]
  51. 51.
    Miziorko HM. 1979. Ribulose-1,5-biphosphate carboxylase. Evidence in support of the existence of distinct CO2 activator and CO2 substrate sites. J. Biol. Chem. 254:270–72
    [Google Scholar]
  52. 52.
    Cooper TG, Filmer D, Wishnick M, Lane MD. 1969. The active species of “CO2” utilized by ribulose diphosphate carboxylase. J. Biol. Chem. 244:1081–83
    [Google Scholar]
  53. 53.
    Saver BG, Knowles JR. 1982. Ribulose 1,5-bisphosphate carboxylase: enzyme-catalyzed appearance of solvent tritium at carbon 3 of ribulose 1,5-bisphosphate reisolated after partial reaction. Biochemistry 21:5398–403
    [Google Scholar]
  54. 54.
    Sue JM, Knowles JR. 1982. Ribulose-1,5-bisphosphate carboxylase: fate of the tritium label in [3-3H]ribulose 1,5-bisphosphate during the enzyme-catalyzed reaction. Biochemistry 21:5404–10
    [Google Scholar]
  55. 55.
    Gutteridge S, Parry MAJ, Schmidt CNG, Feeney J. 1984. An investigation of ribulosebisphosphate carboxylase activity by high resolution 1H NMR. FEBS Lett 170:355–59
    [Google Scholar]
  56. 56.
    Kawashima N, Wildman SG. 1972. Studies on fraction I protein. IV. Mode of inheritance of primary structure in relation to whether chloroplast or nuclear DNA contains the code for a chloroplast protein. Biochim. Biophys. Acta Nucleic Acids Protein Synth. 262:42–49
    [Google Scholar]
  57. 57.
    Chan PH, Wildman SG. 1972. Chloroplast DNA codes for the primary structure of the large subunit of fraction I protein. Biochim. Biophys. Acta Nucleic Acids Protein Synth. 277:677–80
    [Google Scholar]
  58. 58.
    McIntosh L, Poulsen C, Bogorad L. 1980. Chloroplast gene sequence for the large subunit of ribulose bisphosphatecarboxylase of maize. Nature 288:556–60
    [Google Scholar]
  59. 59.
    Niyogi SK, Foote RS, Mural RJ, Larimer FW, Mitra S et al. 1986. Nonessentiality of histidine 291 of Rhodospirillum rubrum ribulose-bisphosphate carboxylase/oxygenase as determined by site-directed mutagenesis. J. Biol. Chem. 261:10087–92
    [Google Scholar]
  60. 60.
    Hartman FC, Soper TS, Niyogi SK, Mural RJ, Foote RS et al. 1987. Function of Lys-166 of Rhodospirillum rubrum ribulosebisphosphate carboxylase/oxygenase as examined by site-directed mutagenesis. J. Biol. Chem. 262:3496–501
    [Google Scholar]
  61. 61.
    Schneider G, Lindqvist Y, Brändén CI, Lorimer G. 1986. Three-dimensional structure of ribulose-1,5-bisphosphate carboxylase/oxygenase from Rhodospirillum rubrum at 2.9 Å resolution. EMBO J 5:3409–15
    [Google Scholar]
  62. 62.
    Chapman MS, Suh SW, Cascio D, Smith WW, Eisenberg D. 1987. Sliding-layer conformational change limited by the quaternary structure of plant RuBisCO. Nature 329:354–56
    [Google Scholar]
  63. 63.
    Sharkey TD. 2022. The discovery of rubisco. J. Exp. Bot. 74:510–19
    [Google Scholar]
  64. 64.
    Li H, Sawaya MR, Tabita FR, Eisenberg D. 2005. Crystal structure of a RuBisCO-like protein from the green sulfur bacterium Chlorobium tepidum. Structure 13:779–89
    [Google Scholar]
  65. 65.
    Andersson I, Knight S, Schneider G, Lindqvist Y, Lundqvist T et al. 1989. Crystal structure of the active site of ribulose-bisphosphate carboxylase. Nature 337:229–34
    [Google Scholar]
  66. 66.
    Schreuder HA, Knight S, Curmi PM, Andersson I, Cascio D et al. 1993. Crystal structure of activated tobacco rubisco complexed with the reaction-intermediate analogue 2-carboxy-arabinitol 1,5-bisphosphate. Protein Sci 2:1136–46
    [Google Scholar]
  67. 67.
    Taylor TC, Andersson I. 1996. Structural transitions during activation and ligand binding in hexadecameric Rubisco inferred from the crystal structure of the activated unliganded spinach enzyme. Nat. Struct. Biol. 3:95–101
    [Google Scholar]
  68. 68.
    Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S. 2007. Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol. Mol. Biol. Rev. 71:576–99
    [Google Scholar]
  69. 69.
    Spreitzer RJ, Salvucci ME. 2002. Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Annu. Rev. Plant Biol. 53:449–75
    [Google Scholar]
  70. 70.
    Andersson I, Backlund A. 2008. Structure and function of Rubisco. Plant Physiol. Biochem. 46:275–91
    [Google Scholar]
  71. 71.
    Wildman SG, Bonner J. 1947. The proteins of green leaves; isolation, enzymatic properties and auxin content of spinach cytoplasmic proteins. Arch. Biochem. 14:381–413
    [Google Scholar]
  72. 72.
    Nishimura M, Takabe T, Sugiyama T, Akazawa T 1973. Structure and function of chloroplast proteins: XIX. Dissociation of spinach leaf ribulose-1,5-diphosphate carboxylase by mercuribenzoate. J. Biochem. 74:945–54
    [Google Scholar]
  73. 73.
    Baker TS, Suh SW, Eisenberg D. 1977. Structure of ribulose-1,5-bisphosphate carboxylase-oxygenase: form III crystals. PNAS 74:1037–41
    [Google Scholar]
  74. 74.
    Badger MR, Bek EJ. 2008. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J. Exp. Bot. 59:1525–41
    [Google Scholar]
  75. 75.
    Andrews TJ. 1988. Catalysis by cyanobacterial ribulose-bisphosphate carboxylase large subunits in the complete absence of small subunits. J. Biol. Chem. 263:12213–19
    [Google Scholar]
  76. 76.
    Spreitzer RJ. 2003. Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. Arch. Biochem. Biophys. 414:141–49
    [Google Scholar]
  77. 77.
    Mao Y, Catherall E, Díaz-Ramos A, Greiff GRL, Azinas S et al. 2022. The small subunit of Rubisco and its potential as an engineering target. J. Exp. Bot. 74:543–61
    [Google Scholar]
  78. 78.
    Mallik S, Goloubinoff P, Tawfik DS. 2021. On the evolution of chaperones and cochaperones and the expansion of proteomes across the Tree of Life. PNAS 118:e2020885118
    [Google Scholar]
  79. 79.
    Banda DM, Pereira JH, Liu AK, Orr DJ, Hammel M et al. 2020. Novel bacterial clade reveals origin of form I Rubisco. Nat. Plants 6:1158–66
    [Google Scholar]
  80. 80.
    Satagopan S, Chan S, Jeanne Perry L, Robert Tabita F 2014. Structure-function studies with the unique hexameric form II ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) from Rhodopseudomonas palustris. J. Biol. Chem. 289:21433–50
    [Google Scholar]
  81. 81.
    Lin MT, Stone WD, Chaudhari V, Hanson MR. 2020. Small subunits can determine enzyme kinetics of tobacco Rubisco expressed in Escherichia coli. Nat. Plants 6:1289–99
    [Google Scholar]
  82. 82.
    He S, Chou H-T, Matthies D, Wunder T, Meyer MT et al. 2020. The structural basis of Rubisco phase separation in the pyrenoid. Nat. Plants 6:1480–90
    [Google Scholar]
  83. 83.
    Oltrogge LM, Chaijarasphong T, Chen AW, Bolin ER, Marqusee S, Savage DF. 2020. Multivalent interactions between CsoS2 and Rubisco mediate α-carboxysome formation. Nat. Struct. Mol. Biol. 27:281–87
    [Google Scholar]
  84. 84.
    Wang H, Yan X, Aigner H, Bracher A, Nguyen ND et al. 2019. Rubisco condensate formation by CcmM in β-carboxysome biogenesis. Nature 566:131–35
    [Google Scholar]
  85. 85.
    Blikstad C, Dugan EJ, Laughlin TG, Liu MD. 2021. Discovery of a carbonic anhydrase-Rubisco supercomplex within the alpha-carboxysome. bioRxiv 2021.11.05.467472. https://doi.org/10.1101/2021.11.05.467472
    [Crossref]
  86. 86.
    Whitney SM, Kane HJ, Houtz RL, Sharwood RE. 2009. Rubisco oligomers composed of linked small and large subunits assemble in tobacco plastids and have higher affinities for CO2 and O2. Plant Physiol 149:1887–95
    [Google Scholar]
  87. 87.
    Bracher A, Whitney SM, Hartl FU, Hayer-Hartl M. 2017. Biogenesis and metabolic maintenance of rubisco. Annu. Rev. Plant Biol. 68:29–60
    [Google Scholar]
  88. 88.
    Aigner H, Wilson RH, Bracher A, Calisse L, Bhat JY et al. 2017. Plant RuBisCo assembly in E. coli with five chloroplast chaperones including BSD2. Science 358:1272–78
    [Google Scholar]
  89. 89.
    Kannappan B, Cummins PL, Gready JE. 2019. Mechanism of oxygenase-pathway reactions catalyzed by rubisco from large-scale Kohn–Sham density functional calculations. J. Phys. Chem. B 123:2833–43
    [Google Scholar]
  90. 90.
    Tcherkez G. 2013. Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/oxygenase and consequences for kinetic parameters. Plant Cell Environ 36:1586–96
    [Google Scholar]
  91. 91.
    Lorimer GH, Andrews TJ, Pierce J, Schloss JV. 1986. 2′-carboxy-3-keto-D-arabinitol 1,5-bisphosphate, the six-carbon intermediate of the ribulose bisphosphate carboxylase reaction. Philos. Trans. R. Soc. B 313:397–407
    [Google Scholar]
  92. 92.
    Cummins PL, Kannappan B, Gready JE. 2018. Revised mechanism of carboxylation of ribulose-1,5-biphosphate by rubisco from large scale quantum chemical calculations. J. Comput. Chem. 39:1656–65
    [Google Scholar]
  93. 93.
    Tcherkez GGB, Bathellier C, Stuart-Williams H, Whitney S, Gout E et al. 2013. D2O solvent isotope effects suggest uniform energy barriers in ribulose-1,5-bisphosphate carboxylase/oxygenase catalysis. Biochemistry 52:869–77
    [Google Scholar]
  94. 94.
    Fried SD, Boxer SG. 2017. Electric fields and enzyme catalysis. Annu. Rev. Biochem. 86:387–415
    [Google Scholar]
  95. 95.
    Kim SM, Lim HS, Lee SB. 2018. Discovery of a RuBisCO-like protein that functions as an oxygenase in the novel d-hamamelose pathway. Biotechnol. Bioprocess Eng. 23:490–99
    [Google Scholar]
  96. 96.
    Robison PD, Martin MN, Tabita FR. 1979. Differential effects of metal ions on Rhodospirillum rubrum ribulosebisphosphate carboxylase/oxygenase and stoichiometric incorporation of HCO3 into a cobalt(III)–enzyme complex. Biochemistry 18:4453–58
    [Google Scholar]
  97. 97.
    Stec B. 2012. Structural mechanism of RuBisCO activation by carbamylation of the active site lysine. PNAS 109:18785–90
    [Google Scholar]
  98. 98.
    Valegård K, Andralojc PJ, Haslam RP, Pearce FG, Eriksen GK et al. 2018. Structural and functional analyses of Rubisco from arctic diatom species reveal unusual posttranslational modifications. J. Biol. Chem. 293:13033–43
    [Google Scholar]
  99. 99.
    Bhat JY, Miličić G, Thieulin-Pardo G, Bracher A, Maxwell A et al. 2017. Mechanism of enzyme repair by the AAA+ chaperone rubisco activase. Mol. Cell 67:744–56.e6
    [Google Scholar]
  100. 100.
    Astier J, Rasul S, Koen E, Manzoor H, Besson-Bard A et al. 2011. S-nitrosylation: an emerging post-translational protein modification in plants. Plant Sci 181:527–33
    [Google Scholar]
  101. 101.
    Gutteridge S, Parry MAJ, Burton S, Keys AJ, Mudd A et al. 1986. A nocturnal inhibitor of carboxylation in leaves. Nature 324:274–76
    [Google Scholar]
  102. 102.
    Khan S, Andralojc PJ, Lea PJ, Parry MAJ. 1999. 2′-Carboxy-D-arabitinol 1-phosphate protects ribulose 1,5-bisphosphate carboxylase/oxygenase against proteolytic breakdown. Eur. J. Biochem. 266:840–47
    [Google Scholar]
  103. 103.
    Jordan DB, Ogren WL. 1981. Species variation in the specificity of ribulose biphosphate carboxylase/oxygenase. Nature 291:513–15
    [Google Scholar]
  104. 104.
    McNevin D, von Caemmerer S, Farquhar G. 2006. Determining RuBisCO activation kinetics and other rate and equilibrium constants by simultaneous multiple non-linear regression of a kinetic model. J. Exp. Bot. 57:3883–900
    [Google Scholar]
  105. 105.
    von Caemmerer S, Evans JR, Hudson GS, Andrews TJ. 1994. The kinetics of ribulose-1,5-bisphosphate carboxylase/oxygenase in vivo inferred from measurements of photosynthesis in leaves of transgenic tobacco. Planta 195:88–97
    [Google Scholar]
  106. 106.
    Iñiguez C, Capó-Bauçà S, Niinemets Ü, Stoll H, Aguiló-Nicolau P, Galmés J. 2020. Evolutionary trends in RuBisCO kinetics and their co-evolution with CO2 concentrating mechanisms. Plant J 101:897–918
    [Google Scholar]
  107. 107.
    Bouvier JW, Emms DM, Rhodes T, Bolton JS, Brasnett A et al. 2021. Rubisco adaptation is more limited by phylogenetic constraint than by catalytic trade-off. Mol. Biol. Evol. 38:2880–96
    [Google Scholar]
  108. 108.
    Tcherkez G, Farquhar GD. 2021. Rubisco catalytic adaptation is mostly driven by photosynthetic conditions – not by phylogenetic constraints. J. Plant Physiol. 267:153554
    [Google Scholar]
  109. 109.
    Tcherkez GG, Bathellier C, Farquhar GD, Lorimer GH. 2018. Commentary: Directions for optimization of photosynthetic carbon fixation: RuBisCO's efficiency may not be so constrained after all. Front. Plant Sci. 9:929
    [Google Scholar]
  110. 110.
    Cummins PL, Kannappan B, Gready JE. 2019. Response: Commentary: Directions for optimization of photosynthetic carbon fixation: RuBisCO's efficiency may not be so constrained after all. Front. Plant Sci. 10:1426
    [Google Scholar]
  111. 111.
    Badger MR, Sharwood RE. 2022. Rubisco, the imperfect winner: “It's all about the base.”. J. Exp. Bot. 74:562–80
    [Google Scholar]
  112. 112.
    Raven JA, Cockell CS, De La, Rocha CL. 2008. The evolution of inorganic carbon concentrating mechanisms in photosynthesis. Philos. Trans. R. Soc. B 363:2641–50
    [Google Scholar]
  113. 113.
    Hennacy JH, Jonikas MC. 2020. Prospects for engineering biophysical CO2 concentrating mechanisms into land plants to enhance yields. Annu. Rev. Plant Biol. 71:461–85
    [Google Scholar]
  114. 114.
    Flamholz AI, Dugan E, Blikstad C, Gleizer S, Ben-Nissan R et al. 2020. Functional reconstitution of a bacterial CO2 concentrating mechanism in Escherichia coli. eLife 9:e59882
    [Google Scholar]
  115. 115.
    Sage RF. 2004. The evolution of C4 photosynthesis. New Phytol 161:341–70
    [Google Scholar]
  116. 116.
    Bar-Even A, Noor E, Milo R. 2012. A survey of carbon fixation pathways through a quantitative lens. J. Exp. Bot. 63:2325–42
    [Google Scholar]
  117. 117.
    Fuchs G. 2011. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?. Annu. Rev. Microbiol. 65:631–58
    [Google Scholar]
  118. 118.
    Bar-Even A, Flamholz A, Noor E, Milo R. 2012. Thermodynamic constraints shape the structure of carbon fixation pathways. Biochim. Biophys. Acta Bioener. 1817:1646–59
    [Google Scholar]
  119. 119.
    Aleku GA, Roberts GW, Titchiner GR, Leys D. 2021. Synthetic enzyme-catalyzed CO2 fixation reactions. ChemSusChem 14:1781–804
    [Google Scholar]
  120. 120.
    Martin J, Eisoldt L, Skerra A. 2018. Fixation of gaseous CO2 by reversing a decarboxylase for the biocatalytic synthesis of the essential amino acid l-methionine. Nat. Catal. 1:555–61
    [Google Scholar]
  121. 121.
    Satanowski A, Dronsella B, Noor E, Vögeli B, He H et al. 2020. Awakening a latent carbon fixation cycle in Escherichia coli. Nat. Commun. 11:5812
    [Google Scholar]
  122. 122.
    Knowles JR. 1989. The mechanism of biotin-dependent enzymes. Annu. Rev. Biochem. 58:195–221
    [Google Scholar]
  123. 123.
    Erb TJ. 2011. Carboxylases in natural and synthetic microbial pathways. Appl. Environ. Microbiol. 77:8466–77
    [Google Scholar]
  124. 124.
    Schwander T, Schada von Borzyskowski L, Burgener S, Cortina NS, Erb TJ. 2016. A synthetic pathway for the fixation of carbon dioxide in vitro. Science 354:900–4
    [Google Scholar]
  125. 125.
    Bar-Even A, Noor E, Lewis NE, Milo R 2010. Design and analysis of synthetic carbon fixation pathways. PNAS 107:8889–94
    [Google Scholar]
  126. 126.
    Zelcbuch L. 2015. Implementing synthetic carbon fixation pathway in the model organism Escherichia Coli. PhD Thesis Weizmann Inst. Sci., Rehovot, Isr https://doi.org/10.34933/WIS.000033
    [Crossref] [Google Scholar]
  127. 127.
    Trudeau DL, Edlich-Muth C, Zarzycki J, Scheffen M, Goldsmith M et al. 2018. Design and in vitro realization of carbon-conserving photorespiration. PNAS 115:E11455–64
    [Google Scholar]
  128. 128.
    Gleizer S, Ben-Nissan R, Bar-On YM, Antonovsky N, Noor E et al. 2019. Conversion of Escherichia coli to generate all biomass carbon from CO2. Cell 179:1255–63.e12
    [Google Scholar]
  129. 129.
    Antonovsky N, Gleizer S, Noor E, Zohar Y, Herz E et al. 2016. Sugar synthesis from CO2 in Escherichia coli. Cell 166:115–25
    [Google Scholar]
  130. 130.
    Watson GM, Yu JP, Tabita FR. 1999. Unusual ribulose 1,5-bisphosphate carboxylase/oxygenase of anoxic Archaea. J. Bacteriol. 181:1569–75
    [Google Scholar]
  131. 131.
    Ezaki S, Maeda N, Kishimoto T, Atomi H, Imanaka T. 1999. Presence of a structurally novel type ribulose-bisphosphate carboxylase/oxygenase in the hyperthermophilic archaeon, Pyrococcus kodakaraensis KOD1. J. Biol. Chem. 274:5078–82
    [Google Scholar]
  132. 132.
    Liu D, Ramya RCS, Mueller-Cajar O. 2017. Surveying the expanding prokaryotic Rubisco multiverse. FEMS Microbiol. Lett. 364:fnx156
    [Google Scholar]
  133. 133.
    Schwender J, Goffman F, Ohlrogge JB, Shachar-Hill Y. 2004. Rubisco without the Calvin cycle improves the carbon efficiency of developing green seeds. Nature 432:779–82
    [Google Scholar]
  134. 134.
    Wrighton KC, Castelle CJ, Varaljay VA, Satagopan S, Brown CT et al. 2016. RubisCO of a nucleoside pathway known from Archaea is found in diverse uncultivated phyla in bacteria. ISME J 10:2702–14
    [Google Scholar]
  135. 135.
    Sato T, Atomi H, Imanaka T. 2007. Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315:1003–6
    [Google Scholar]
  136. 136.
    Kono T, Mehrotra S, Endo C, Kizu N, Matusda M et al. 2017. A RuBisCO-mediated carbon metabolic pathway in methanogenic archaea. Nat. Commun. 8:14007
    [Google Scholar]
  137. 137.
    Frolov EN, Kublanov IV, Toshchakov SV, Lunev EA, Pimenov NV et al. 2019. Form III RubisCO-mediated transaldolase variant of the Calvin cycle in a chemolithoautotrophic bacterium. PNAS 116:18638–46
    [Google Scholar]
  138. 138.
    Jaffe AL, Castelle CJ, Dupont CL, Banfield JF. 2019. Lateral gene transfer shapes the distribution of RuBisCO among candidate phyla radiation bacteria and DPANN archaea. Mol. Biol. Evol. 36:435–46
    [Google Scholar]
  139. 139.
    Hanson TE, Tabita FR. 2001. A ribulose-1,5-bisphosphate carboxylase/oxygenase (RubisCO)-like protein from Chlorobium tepidum that is involved with sulfur metabolism and the response to oxidative stress. PNAS 98:4397–402
    [Google Scholar]
  140. 140.
    Carter MS, Zhang X, Huang H, Bouvier JT, Francisco BS et al. 2018. Functional assignment of multiple catabolic pathways for D-apiose. Nat. Chem. Biol. 14:696–705
    [Google Scholar]
  141. 141.
    Kreel NE, Tabita FR. 2007. Substitutions at methionine 295 of Archaeoglobus fulgidus ribulose-1,5-bisphosphate carboxylase/oxygenase affect oxygen binding and CO2/O2 specificity. J. Biol. Chem. 282:1341–51
    [Google Scholar]
  142. 142.
    Dey S, North JA, Sriram J, Evans BS, Tabita FR. 2015. In vivo studies in Rhodospirillum rubrum indicate that ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) catalyzes two obligatorily required and physiologically significant reactions for distinct carbon and sulfur metabolic pathways. J. Biol. Chem. 290:30658–68
    [Google Scholar]
  143. 143.
    Erb TJ, Zarzycki J. 2018. A short history of RubisCO: the rise and fall (?) of Nature's predominant CO2 fixing enzyme. Curr. Opin. Biotechnol. 49:100–7
    [Google Scholar]
  144. 144.
    Bouvier JW, Emms DM, Kelly S. 2022. Slow molecular evolution of rubisco limits adaptive improvement of CO2 assimilation. bioRxiv 2022.07.06.498985. http://doi.org/10.1101/2022.07.06.498985
    [Crossref]
  145. 145.
    Delwiche CF, Palmer JD. 1996. Rampant horizontal transfer and duplication of rubisco genes in eubacteria and plastids. Mol. Biol. Evol. 13:873–82
    [Google Scholar]
  146. 146.
    Whitney SM, Shaw DC, Yellowlees D. 1995. Evidence that some dinoflagellates contain a ribulose-1,5-bisphosphate carboxylase/oxygenase related to that of the α-proteobacteria. Proc. Biol. Sci. 259:271–75
    [Google Scholar]
  147. 147.
    West-Roberts JA, Matheus-Carnevali PB, Schoelmerich MC, Al-Shayeb B, Thomas AD et al. 2021. The Chloroflexi supergroup is metabolically diverse and representatives have novel genes for non-photosynthesis based CO2 fixation. bioRxiv 2021.08.23.457424. http://doi.org/10.1101/2021.08.23.457424
    [Crossref]
  148. 148.
    Schulz L, Guo Z, Zarzycki J, Steinchen W, Schuller JM et al. 2022. Evolution of increased complexity and specificity at the dawn of form I Rubiscos. Science 378:155–60
    [Google Scholar]
  149. 149.
    Varaljay VA, Satagopan S, North JA, Witte B, Dourado MN et al. 2016. Functional metagenomic selection of ribulose 1,5-bisphosphate carboxylase/oxygenase from uncultivated bacteria. Environ. Microbiol. 18:1187–99
    [Google Scholar]
  150. 150.
    Böhnke S, Perner M. 2015. A function-based screen for seeking RubisCO active clones from metagenomes: novel enzymes influencing RubisCO activity. ISME J 9:735–45
    [Google Scholar]
  151. 151.
    Witte B, John D, Wawrik B, Paul JH, Dayan D, Tabita FR. 2010. Functional prokaryotic RubisCO from an oceanic metagenomic library. Appl. Environ. Microbiol. 76:2997–3003
    [Google Scholar]
  152. 152.
    Spreitzer RJ, Peddi SR, Satagopan S. 2005. Phylogenetic engineering at an interface between large and small subunits imparts land-plant kinetic properties to algal Rubisco. PNAS 102:17225–30
    [Google Scholar]
  153. 153.
    Higgins SA, Savage DF. 2018. Protein science by DNA sequencing: how advances in molecular biology are accelerating biochemistry. Biochemistry 57:38–46
    [Google Scholar]
  154. 154.
    Lu H, Diaz DJ, Czarnecki NJ, Zhu C, Kim W et al. 2022. Machine learning-aided engineering of hydrolases for PET depolymerization. Nature 604:662–67
    [Google Scholar]
  155. 155.
    Bryant DH, Bashir A, Sinai S, Jain NK, Ogden PJ et al. 2021. Deep diversification of an AAV capsid protein by machine learning. Nat. Biotechnol. 39:691–96
    [Google Scholar]
  156. 156.
    Iqbal WA, Lisitsa A, Kapralov MV. 2022. Predicting plant Rubisco kinetics from RbcL sequence data using machine learning. J. Exp. Bot. 74:638–50
    [Google Scholar]
  157. 157.
    Paoli GC, Vichivanives P, Tabita FR. 1998. Physiological control and regulation of the Rhodobacter capsulatus cbb operons. J. Bacteriol. 180:4258–69
    [Google Scholar]
  158. 158.
    Satagopan S, North JA, Arbing MA, Varaljay VA, Haines SN et al. 2019. Structural perturbations of Rhodopseudomonas palustris form II RuBisCO mutant enzymes that affect CO2 fixation. Biochemistry 58:3880–92
    [Google Scholar]
  159. 159.
    Yoshida S, Atomi H, Imanaka T. 2007. Engineering of a type III rubisco from a hyperthermophilic archaeon in order to enhance catalytic performance in mesophilic host cells. Appl. Environ. Microbiol. 73:6254–61
    [Google Scholar]
  160. 160.
    Satagopan S, Tabita FR. 2016. RubisCO selection using the vigorously aerobic and metabolically versatile bacterium Ralstonia eutropha. FEBS J 283:2869–80
    [Google Scholar]
  161. 161.
    Parikh MR, Greene DN, Woods KK, Matsumura I. 2006. Directed evolution of RuBisCO hypermorphs through genetic selection in engineered E. coli. Protein Eng. Des. Sel. 19:113–19
    [Google Scholar]
  162. 162.
    Wilson RH, Martin-Avila E, Conlan C, Whitney SM. 2018. An improved Escherichia coli screen for Rubisco identifies a protein–protein interface that can enhance CO2-fixation kinetics. J. Biol. Chem. 293:18–27
    [Google Scholar]
  163. 163.
    Zhou Y, Whitney S. 2019. Directed evolution of an improved rubisco; in vitro analyses to decipher fact from fiction. Int. J. Mol. Sci. 20:5019
    [Google Scholar]
  164. 164.
    Mueller-Cajar O, Morell M, Whitney SM. 2007. Directed evolution of rubisco in Escherichia coli reveals a specificity-determining hydrogen bond in the form II enzyme. Biochemistry 46:14067–74
    [Google Scholar]
  165. 165.
    Aslan S, Noor E, Benito Vaquerizo S, Lindner SN, Bar-Even A 2020. Design and engineering of E. coli metabolic sensor strains with a wide sensitivity range for glycerate. Metab. Eng. 57:96–109
    [Google Scholar]
  166. 166.
    Svab Z, Maliga P. 1993. High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. PNAS 90:913–17
    [Google Scholar]
  167. 167.
    Kanevski I, Maliga P. 1994. Relocation of the plastid rbcL gene to the nucleus yields functional ribulose-1,5-bisphosphate carboxylase in tobacco chloroplasts. PNAS 91:1969–73
    [Google Scholar]
  168. 168.
    Lin MT, Occhialini A, Andralojc PJ, Parry MAJ, Hanson MR. 2014. A faster Rubisco with potential to increase photosynthesis in crops. Nature 513:547–50
    [Google Scholar]
  169. 169.
    Occhialini A, Lin MT, Andralojc PJ, Hanson MR, Parry MAJ. 2016. Transgenic tobacco plants with improved cyanobacterial Rubisco expression but no extra assembly factors grow at near wild-type rates if provided with elevated CO2. Plant J 85:148–160
    [Google Scholar]
  170. 170.
    Martin-Avila E, Lim Y-L, Birch R, Dirk LMA, Buck S et al. 2020. Modifying plant photosynthesis and growth via simultaneous chloroplast transformation of rubisco large and small subunits. Plant Cell 32:2898–916
    [Google Scholar]
  171. 171.
    Whitney SM, Andrews TJ. 2003. Photosynthesis and growth of tobacco with a substituted bacterial Rubisco mirror the properties of the introduced enzyme. Plant Physiol 133:287–94
    [Google Scholar]
  172. 172.
    Yoon D-K, Ishiyama K, Suganami M, Tazoe Y, Watanabe M et al. 2020. Transgenic rice overproducing Rubisco exhibits increased yields with improved nitrogen-use efficiency in an experimental paddy field. Nat. Food 1:134–39
    [Google Scholar]
  173. 173.
    Salesse-Smith CE, Sharwood RE, Busch FA, Kromdijk J, Bardal V, Stern DB. 2018. Overexpression of Rubisco subunits with RAF1 increases Rubisco content in maize. Nat. Plants 4:802–10
    [Google Scholar]
  174. 174.
    Lin MT, Hanson MR 2018. Red algal Rubisco fails to accumulate in transplastomic tobacco expressing Griffithsia monilis RbcL and RbcS genes. Plant Direct. 2:e00045
    [Google Scholar]
  175. 175.
    Gunn LH, Martin Avila E, Birch R, Whitney SM 2020. The dependency of red Rubisco on its cognate activase for enhancing plant photosynthesis and growth. PNAS 117:25890–96
    [Google Scholar]
  176. 176.
    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. Plant J 26:535–47
    [Google Scholar]
  177. 177.
    Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE et al. 2015. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. PNAS 112:8529–36
    [Google Scholar]
  178. 178.
    South PF, Cavanagh AP, Liu HW, Ort DR. 2019. Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science 363:eaat9077
    [Google Scholar]
  179. 179.
    Driever SM, Simkin AJ, Alotaibi S, Fisk SJ, Madgwick PJ et al. 2017. Increased SBPase activity improves photosynthesis and grain yield in wheat grown in greenhouse conditions. Philos. Trans. R. Soc. B 372:20160384
    [Google Scholar]
  180. 180.
    Long BM, Hee WY, Sharwood RE, Rae BD, Kaines S et al. 2018. Carboxysome encapsulation of the CO2-fixing enzyme Rubisco in tobacco chloroplasts. Nat. Commun. 9:3570
    [Google Scholar]
/content/journals/10.1146/annurev-biochem-040320-101244
Loading
/content/journals/10.1146/annurev-biochem-040320-101244
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error