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The crystal structure of rubisco from Alcaligenes eutrophus reveals a novel central eight-stranded beta-barrel formed by beta-strands from four subunits.

Hansen S, Vollan VB, Hough E, Andersen K
J Mol Biol 288 609-21 (1999)
Cited: 39 times
EuropePMC logo PMID: 10329167

Abstract

Ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco) is involved in photosynthesis where it catalyzes the initial step in the fixation of carbon dioxide. The enzyme also catalyzes a competing oxygenation reaction leading to loss of fixed carbon dioxide, thus reducing the net efficiency of photosynthesis significantly. Rubisco has therefore been studied extensively, and a challenging goal is the engineering of a more photosynthetically efficient enzyme. Hexadecameric rubiscos fall in two distinct groups, "green-like" and "red-like". The ability to discriminate between CO2 and O2 as substrates varies significantly, and some algae have red-like rubisco with even higher specificity for CO2 than the plant enzyme. The structure of unactivated rubisco from Alcaligenes eutrophus has been determined to 2.7 A resolution by molecular replacement and refined to R and Rfree values of 26.6 and 32.2 %, respectively. The overall fold of the protein is very similar to the rubisco structures solved previously for green-like hexadecameric enzymes, except for the extended C-terminal domains of the small subunits which together form an eight-stranded beta-barrel which sits as a plug in the entrance to the central solvent channel in the molecule. The present structure is the first which has been solved for a red-like rubisco and is likely to represent a fold which is common for this group. The small subunits in general are believed to have a stabilizing effect, and the new quaternary structure in the oligomer of the present structure is likely to contribute even more to this stabilization of the assembled rubisco protein.

Reviews - 1bxn mentioned but not cited (4)

  1. The Diverse AAA+ Machines that Repair Inhibited Rubisco Active Sites. Mueller-Cajar O. Front Mol Biosci 4 31 (2017)
  2. The small subunit of Rubisco and its potential as an engineering target. Mao Y, Catherall E, Díaz-Ramos A, Greiff GRL, Azinas S, Gunn L, McCormick AJ. J Exp Bot 74 543-561 (2023)
  3. Red Rubiscos and opportunities for engineering green plants. Oh ZG, Askey B, Gunn LH. J Exp Bot 74 520-542 (2023)
  4. Clearing the air: unraveling past and guiding future research in atmospheric chemosynthesis. Ray AE, Tribbia DZ, Cowan DA, Ferrari BC. Microbiol Mol Biol Rev 87 e0004823 (2023)

Articles - 1bxn mentioned but not cited (14)

  1. A structural model for the damage-sensing complex in bacterial nucleotide excision repair. Pakotiprapha D, Liu Y, Verdine GL, Jeruzalmi D. J Biol Chem 284 12837-12844 (2009)
  2. Characterization of the heterooligomeric red-type rubisco activase from red algae. Loganathan N, Tsai YC, Mueller-Cajar O. Proc Natl Acad Sci U S A 113 14019-14024 (2016)
  3. The small RbcS-like domains of the β-carboxysome structural protein CcmM bind RubisCO at a site distinct from that binding the RbcS subunit. Ryan P, Forrester TJB, Wroblewski C, Kenney TMG, Kitova EN, Klassen JS, Kimber MS. J Biol Chem 294 2593-2603 (2019)
  4. Role of small subunit in mediating assembly of red-type form I Rubisco. Joshi J, Mueller-Cajar O, Tsai YC, Hartl FU, Hayer-Hartl M. J Biol Chem 290 1066-1074 (2015)
  5. Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree. Kacar B, Hanson-Smith V, Adam ZR, Boekelheide N. Geobiology 15 628-640 (2017)
  6. RubisCO selection using the vigorously aerobic and metabolically versatile bacterium Ralstonia eutropha. Satagopan S, Tabita FR. FEBS J 283 2869-2880 (2016)
  7. Structure of Rubisco from Arabidopsis thaliana in complex with 2-carboxyarabinitol-1,5-bisphosphate. Valegård K, Hasse D, Andersson I, Gunn LH. Acta Crystallogr D Struct Biol 74 1-9 (2018)
  8. 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)
  9. Synthetic CO2-fixation enzyme cascades immobilized on self-assembled nanostructures that enhance CO2/O2 selectivity of RubisCO. Satagopan S, Sun Y, Parquette JR, Tabita FR. Biotechnol Biofuels 10 175 (2017)
  10. Macromolecules Structural Classification With a 3D Dilated Dense Network in Cryo-Electron Tomography. Gao S, Han R, Zeng X, Liu Z, Xu M, Zhang F. IEEE/ACM Trans Comput Biol Bioinform 19 209-219 (2022)
  11. Structural Analysis of SMYD3 Lysine Methyltransferase for the Development of Competitive and Specific Enzyme Inhibitors. Jarrell DK, Hassell KN, Alshiraihi I, Crans DC, Brown MA. Diseases 10 4 (2021)
  12. Dilated-DenseNet For Macromolecule Classification In Cryo-electron Tomography. Gao S, Han R, Zeng X, Cui X, Liu Z, Xu M, Zhang F. Bioinform Res Appl 12304 82-94 (2020)
  13. FSCC: Few-Shot Learning for Macromolecule Classification Based on Contrastive Learning and Distribution Calibration in Cryo-Electron Tomography. Gao S, Zeng X, Xu M, Zhang F. Front Mol Biosci 9 931949 (2022)
  14. TomoTwin: generalized 3D localization of macromolecules in cryo-electron tomograms with structural data mining. Rice G, Wagner T, Stabrin M, Sitsel O, Prumbaum D, Raunser S. Nat Methods 20 871-880 (2023)


Reviews citing this publication (5)

  1. Rubisco: structure, regulatory interactions, and possibilities for a better enzyme. Spreitzer RJ, Salvucci ME. Annu Rev Plant Biol 53 449-475 (2002)
  2. Structure and function of Rubisco. Andersson I, Backlund A. Plant Physiol Biochem 46 275-291 (2008)
  3. Role of the small subunit in ribulose-1,5-bisphosphate carboxylase/oxygenase. Spreitzer RJ. Arch Biochem Biophys 414 141-149 (2003)
  4. Biogenesis and Metabolic Maintenance of Rubisco. Bracher A, Whitney SM, Hartl FU, Hayer-Hartl M. Annu Rev Plant Biol 68 29-60 (2017)
  5. Structural framework for catalysis and regulation in ribulose-1,5-bisphosphate carboxylase/oxygenase. Andersson I, Taylor TC. Arch Biochem Biophys 414 130-140 (2003)

Articles citing this publication (16)

  1. Form I Rubiscos from non-green algae are expressed abundantly but not assembled in tobacco chloroplasts. Whitney SM, Baldet P, Hudson GS, Andrews TJ. Plant J 26 535-547 (2001)
  2. Catalytic by-product formation and ligand binding by ribulose bisphosphate carboxylases from different phylogenies. Pearce FG. Biochem J 399 525-534 (2006)
  3. Crystal structure of a novel-type archaeal rubisco with pentagonal symmetry. Kitano K, Maeda N, Fukui T, Atomi H, Imanaka T, Miki K. Structure 9 473-481 (2001)
  4. Proline alleviates salt-stress-induced enhancement in ribulose-1, 5-bisphosphate oxygenase activity. Sivakumar P, Sharmila P, Pardha Saradhi P. Biochem Biophys Res Commun 279 512-515 (2000)
  5. Microbial enzymes involved in carbon dioxide fixation. Atomi H. J Biosci Bioeng 94 497-505 (2002)
  6. Highly conserved small subunit residues influence rubisco large subunit catalysis. Genkov T, Spreitzer RJ. J Biol Chem 284 30105-30112 (2009)
  7. Visualizing Individual RuBisCO and Its Assembly into Carboxysomes in Marine Cyanobacteria by Cryo-Electron Tomography. Dai W, Chen M, Myers C, Ludtke SJ, Pettitt BM, King JA, Schmid MF, Chiu W. J Mol Biol 430 4156-4167 (2018)
  8. Crystal structure of activated ribulose-1,5-bisphosphate carboxylase/oxygenase from green alga Chlamydomonas reinhardtii complexed with 2-carboxyarabinitol-1,5-bisphosphate. Mizohata E, Matsumura H, Okano Y, Kumei M, Takuma H, Onodera J, Kato K, Shibata N, Inoue T, Yokota A, Kai Y. J Mol Biol 316 679-691 (2002)
  9. Crystal structure of a RuBisCO-like protein from the green sulfur bacterium Chlorobium tepidum. Li H, Sawaya MR, Tabita FR, Eisenberg D. Structure 13 779-789 (2005)
  10. Phylogeny and functional expression of ribulose 1,5-bisphosphate carboxylase/oxygenase from the autotrophic ammonia-oxidizing bacterium Nitrosospira sp. isolate 40KI. Utåker JB, Andersen K, Aakra A, Moen B, Nes IF. J Bacteriol 184 468-478 (2002)
  11. 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)
  12. Sugars have potential to curtail oxygenase activity of Rubisco. Sivakumar P, Sharmila P, Jain V, Pardha Saradhi P. Biochem Biophys Res Commun 298 247-250 (2002)
  13. X-ray structure of Galdieria Rubisco complexed with one sulfate ion per active site. Okano Y, Mizohata E, Xie Y, Matsumura H, Sugawara H, Inoue T, Yokota A, Kai Y. FEBS Lett 527 33-36 (2002)
  14. Ribulose-1,5-bisphosphate carboxylase/oxygenase from thermophilic cyanobacterium Thermosynechococcus elongatus. Gubernator B, Bartoszewski R, Kroliczewski J, Wildner G, Szczepaniak A. Photosynth Res 95 101-109 (2008)
  15. Substitutions at the opening of the Rubisco central solvent channel affect holoenzyme stability and CO2/O 2 specificity but not activation by Rubisco activase. Esquivel MG, Genkov T, Nogueira AS, Salvucci ME, Spreitzer RJ. Photosynth Res 118 209-218 (2013)
  16. Deletion of nine carboxy-terminal residues of the Rubisco small subunit decreases thermal stability but does not eliminate function. Esquível MG, Anwaruzzaman M, Spreitzer RJ. FEBS Lett 520 73-76 (2002)


Related citations provided by authors (1)

  1. Purification, Crystallization and Preliminary X-Ray Studies of Two Isoforms of Rubisco from Alcaligenes Eutrophus. Hansen S, Hough E, Andersen K Acta Crystallogr. D Biol. Crystallogr. 55 310- (1999)

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