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Structural mechanism of RuBisCO activation by carbamylation of the active site lysine.

Stec B
Proc Natl Acad Sci U S A 109 18785-90 (2012)
Related entries: 4f0k, 4f0m

Cited: 37 times
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Abstract

Ribulose 1,5-bisphosphate carboxylase/oxygenase (RuBisCO) is a crucial enzyme in carbon fixation and the most abundant protein on earth. It has been studied extensively by biochemical and structural methods; however, the most essential activation step has not yet been described. Here, we describe the mechanistic details of Lys carbamylation that leads to RuBisCO activation by atmospheric CO(2). We report two crystal structures of nitrosylated RuBisCO from the red algae Galdieria sulphuraria with O(2) and CO(2) bound at the active site. G. sulphuraria RuBisCO is inhibited by cysteine nitrosylation that results in trapping of these gaseous ligands. The structure with CO(2) defines an elusive, preactivation complex that contains a metal cation Mg(2+) surrounded by three H(2)O/OH molecules. Both structures suggest the mechanism for discriminating gaseous ligands by their quadrupole electric moments. We describe conformational changes that allow for intermittent binding of the metal ion required for activation. On the basis of these structures we propose the individual steps of the activation mechanism. Knowledge of all these elements is indispensable for engineering RuBisCO into a more efficient enzyme for crop enhancement or as a remedy to global warming.

Reviews - 4f0h mentioned but not cited (1)

  1. Red Rubiscos and opportunities for engineering green plants. Oh ZG, Askey B, Gunn LH. J Exp Bot 74 520-542 (2023)

Articles - 4f0h mentioned but not cited (4)

  1. Structural mechanism of RuBisCO activation by carbamylation of the active site lysine. Stec B. Proc Natl Acad Sci U S A 109 18785-18790 (2012)
  2. Comparison of Protein Extracts from Various Unicellular Green Sources. Teuling E, Wierenga PA, Schrama JW, Gruppen H. J Agric Food Chem 65 7989-8002 (2017)
  3. Letter Reply to Kiser: Dioxygen binding in NOV1 crystal structures. McAndrew RP, Sathitsuksanoh N, Mbughuni MM, Heins RA, Pereira JH, George A, Sale KL, Fox BG, Simmons BA, Adams PD. Proc Natl Acad Sci U S A 114 E6029-E6030 (2017)
  4. PTM-Psi: A python package to facilitate the computational investigation of post-translational modification on protein structures and their impacts on dynamics and functions. Mejia-Rodriguez D, Kim H, Sadler N, Li X, Bohutskyi P, Valiev M, Qian WJ, Cheung MS. Protein Sci 32 e4822 (2023)


Reviews citing this publication (11)

  1. Evolutionary development of redox regulation in chloroplasts. Balsera M, Uberegui E, Schürmann P, Buchanan BB. Antioxid Redox Signal 21 1327-1355 (2014)
  2. Effect of posttranslational modifications on enzyme function and assembly. Ryšlavá H, Doubnerová V, Kavan D, Vaněk O. J Proteomics 92 80-109 (2013)
  3. From cyanochemicals to cyanofactories: a review and perspective. Zhou J, Zhu T, Cai Z, Li Y. Microb Cell Fact 15 2 (2016)
  4. Rubisco Activases: AAA+ Chaperones Adapted to Enzyme Repair. Bhat JY, Thieulin-Pardo G, Hartl FU, Hayer-Hartl M. Front Mol Biosci 4 20 (2017)
  5. Photorespiration: The Futile Cycle? Shi X, Bloom A. Plants (Basel) 10 908 (2021)
  6. From chaperonins to Rubisco assembly and metabolic repair. Hayer-Hartl M. Protein Sci 26 2324-2333 (2017)
  7. Carbon Dioxide and the Carbamate Post-Translational Modification. Blake LI, Cann MJ. Front Mol Biosci 9 825706 (2022)
  8. New Trends in Bioremediation Technologies Toward Environment-Friendly Society: A Mini-Review. Dutta K, Shityakov S, Khalifa I. Front Bioeng Biotechnol 9 666858 (2021)
  9. Recent Advances in the Chemistry of Metal Carbamates. Bresciani G, Biancalana L, Pampaloni G, Marchetti F. Molecules 25 E3603 (2020)
  10. Biocatalytic C-C Bond Formation for One Carbon Resource Utilization. Yang Q, Guo X, Liu Y, Jiang H. Int J Mol Sci 22 1890 (2021)
  11. Molecular mechanism of Rubisco activase: Dynamic assembly and Rubisco remodeling. Waheeda K, Kitchel H, Wang Q, Chiu PL. Front Mol Biosci 10 1125922 (2023)

Articles citing this publication (21)

  1. Development of an activity-directed selection system enabled significant improvement of the carboxylation efficiency of Rubisco. Cai Z, Liu G, Zhang J, Li Y. Protein Cell 5 552-562 (2014)
  2. A pangenomic analysis of the Nannochloropsis organellar genomes reveals novel genetic variations in key metabolic genes. Starkenburg SR, Kwon KJ, Jha RK, McKay C, Jacobs M, Chertkov O, Twary S, Rocap G, Cattolico RA. BMC Genomics 15 212 (2014)
  3. Enantioselective small molecule synthesis by carbon dioxide fixation using a dual Brønsted acid/base organocatalyst. Vara BA, Struble TJ, Wang W, Dobish MC, Johnston JN. J Am Chem Soc 137 7302-7305 (2015)
  4. Synechocystis PCC 6803 overexpressing RuBisCO grow faster with increased photosynthesis. Liang F, Lindblad P. Metab Eng Commun 4 29-36 (2017)
  5. Diel magnesium fluctuations in chloroplasts contribute to photosynthesis in rice. Li J, Yokosho K, Liu S, Cao HR, Yamaji N, Zhu XG, Liao H, Ma JF, Chen ZC. Nat Plants 6 848-859 (2020)
  6. High reactivity of deep biota under anthropogenic CO2 injection into basalt. Trias R, Ménez B, le Campion P, Zivanovic Y, Lecourt L, Lecoeuvre A, Schmitt-Kopplin P, Uhl J, Gislason SR, Alfreðsson HA, Mesfin KG, Snæbjörnsdóttir SÓ, Aradóttir ES, Gunnarsson I, Matter JM, Stute M, Oelkers EH, Gérard E. Nat Commun 8 1063 (2017)
  7. Structural and functional analyses of Rubisco from arctic diatom species reveal unusual posttranslational modifications. Valegård K, Andralojc PJ, Haslam RP, Pearce FG, Eriksen GK, Madgwick PJ, Kristoffersen AK, van Lun M, Klein U, Eilertsen HC, Parry MAJ, Andersson I. J Biol Chem 293 13033-13043 (2018)
  8. Serine 363 of a Hydrophobic Region of Archaeal Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase from Archaeoglobus fulgidus and Thermococcus kodakaraensis Affects CO2/O2 Substrate Specificity and Oxygen Sensitivity. Kreel NE, Tabita FR. PLoS One 10 e0138351 (2015)
  9. Biophysical analysis of the structural evolution of substrate specificity in RuBisCO. Poudel S, Pike DH, Raanan H, Mancini JA, Nanda V, Rickaby REM, Falkowski PG. Proc Natl Acad Sci U S A 117 30451-30457 (2020)
  10. An amino acid based system for CO2 capture and catalytic utilization to produce formates. Wei D, Junge H, Beller M. Chem Sci 12 6020-6024 (2021)
  11. Four amino acids define the CO2 binding pocket of enoyl-CoA carboxylases/reductases. Stoffel GMM, Saez DA, DeMirci H, Vögeli B, Rao Y, Zarzycki J, Yoshikuni Y, Wakatsuki S, Vöhringer-Martinez E, Erb TJ. Proc Natl Acad Sci U S A 116 13964-13969 (2019)
  12. Identification of Two bZIP Transcription Factors Interacting with the Promoter of Soybean Rubisco Activase Gene (GmRCAα). Zhang J, Du H, Chao M, Yin Z, Yang H, Li Y, Huang F, Yu D. Front Plant Sci 7 628 (2016)
  13. Effects of aqueous stable fullerene nanocrystal (nC60) on Scenedesmus obliquus: evaluation of the sub-lethal photosynthetic responses and inhibition mechanism. Tao X, Yu Y, Fortner JD, He Y, Chen Y, Hughes JB. Chemosphere 122 162-167 (2015)
  14. Metal Homeostasis and Gas Exchange Dynamics in Pisum sativum L. Exposed to Cerium Oxide Nanoparticles. Skiba E, Pietrzak M, Gapińska M, Wolf WM. Int J Mol Sci 21 E8497 (2020)
  15. Photosynthetic and Growth Responses in a Pioneer Tree (Japanese White Birch) and Competitive Perennial Weeds (Eupatorium sp.) Grown Under Different Regimes With Limited Water Supply to Waterlogging. Kitao M, Harayama H, Yazaki K, Tobita H, Agathokleous E, Furuya N, Hashimoto T. Front Plant Sci 13 835068 (2022)
  16. An Insight of RuBisCO Evolution through a Multilevel Approach. Camel V, Zolla G. Biomolecules 11 1761 (2021)
  17. Chemoproteomic identification of CO2-dependent lysine carboxylation in proteins. King DT, Zhu S, Hardie DB, Serrano-Negrón JE, Madden Z, Kolappan S, Vocadlo DJ. Nat Chem Biol 18 782-791 (2022)
  18. Amino acids downregulate SIRT4 to detoxify ammonia through the urea cycle. Hu SH, Feng YY, Yang YX, Ma HD, Zhou SX, Qiao YN, Zhang KH, Zhang L, Huang L, Yuan YY, Lin Y, Zhang XY, Li Y, Li HT, Zhao JY, Xu W, Zhao SM. Nat Metab 5 626-641 (2023)
  19. Catch your breath. Grams RJ, Hsu KL. Nat Chem Biol 18 686-687 (2022)
  20. Experimental evidence for extra proton exchange in ribulose 1,5-bisphosphate carboxylase/oxygenase catalysis. Bathellier C, Tcherkez G. Commun Integr Biol 15 68-74 (2022)
  21. TMT-Based Proteomic Analysis of Continuous Cropping Response in Codonopsis tangshen Oliv. Jiang X, Zhou W, Wang H, You J, Liu W, Zhang M. Life (Basel) 13 765 (2023)


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