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ATP-induced conformational dynamics in the AAA+ motor unit of magnesium chelatase.

Lundqvist J, Elmlund H, Wulff RP, Berglund L, Elmlund D, Emanuelsson C, Hebert H, Willows RD, Hansson M, Lindahl M, Al-Karadaghi S
Structure 18 354-65 (2010)
Cited: 40 times
EuropePMC logo PMID: 20223218

Abstract

Mg-chelatase catalyzes the first committed step of the chlorophyll biosynthetic pathway, the ATP-dependent insertion of Mg(2+) into protoporphyrin IX (PPIX). Here we report the reconstruction using single-particle cryo-electron microscopy of the complex between subunits BchD and BchI of Rhodobacter capsulatus Mg-chelatase in the presence of ADP, the nonhydrolyzable ATP analog AMPPNP, and ATP at 7.5 A, 14 A, and 13 A resolution, respectively. We show that the two AAA+ modules of the subunits form a unique complex of 3 dimers related by a three-fold axis. The reconstructions demonstrate substantial differences between the conformations of the complex in the presence of ATP and ADP, and suggest that the C-terminal integrin-I domains of the BchD subunits play a central role in transmitting conformational changes of BchI to BchD. Based on these data a model for the function of magnesium chelatase is proposed.

Articles - 2x31 mentioned but not cited (3)

  1. Hexameric structure of the ATPase motor subunit of magnesium chelatase in chlorophyll biosynthesis. Gao YS, Wang YL, Wang X, Liu L. Protein Sci 29 1040-1046 (2020)
  2. The CoxD protein, a novel AAA+ ATPase involved in metal cluster assembly: hydrolysis of nucleotide-triphosphates and oligomerization. Maisel T, Joseph S, Mielke T, Bürger J, Schwarzinger S, Meyer O. PLoS One 7 e47424 (2012)
  3. Dual Reversible Coumarin Inhibitors Mutually Bound to Monoamine Oxidase B and Acetylcholinesterase Crystal Structures. Ekström F, Gottinger A, Forsgren N, Catto M, Iacovino LG, Pisani L, Binda C. ACS Med Chem Lett 13 499-506 (2022)


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  1. Chlorophyll modifications and their spectral extension in oxygenic photosynthesis. Chen M. Annu Rev Biochem 83 317-340 (2014)
  2. Post-translational control of tetrapyrrole biosynthesis in plants, algae, and cyanobacteria. Czarnecki O, Grimm B. J Exp Bot 63 1675-1687 (2012)
  3. Novel structural and functional insights into the MoxR family of AAA+ ATPases. Wong KS, Houry WA. J Struct Biol 179 211-221 (2012)

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  2. SIMPLE: Software for ab initio reconstruction of heterogeneous single-particles. Elmlund D, Elmlund H. J Struct Biol 180 420-427 (2012)
  3. Chlorophyll biosynthesis gene evolution indicates photosystem gene duplication, not photosystem merger, at the origin of oxygenic photosynthesis. Sousa FL, Shavit-Grievink L, Allen JF, Martin WF. Genome Biol Evol 5 200-216 (2013)
  4. Ab initio structure determination from electron microscopic images of single molecules coexisting in different functional states. Elmlund D, Davis R, Elmlund H. Structure 18 777-786 (2010)
  5. Crystal structure of the catalytic subunit of magnesium chelatase. Chen X, Pu H, Fang Y, Wang X, Zhao S, Lin Y, Zhang M, Dai HE, Gong W, Liu L. Nat Plants 1 15125 (2015)
  6. Virus-induced gene silencing of pea CHLI and CHLD affects tetrapyrrole biosynthesis, chloroplast development and the primary metabolic network. Luo T, Luo S, Araújo WL, Schlicke H, Rothbart M, Yu J, Fan T, Fernie AR, Grimm B, Luo M. Plant Physiol Biochem 65 17-26 (2013)
  7. C-terminal residues of oryza sativa GUN4 are required for the activation of the ChlH subunit of magnesium chelatase in chlorophyll synthesis. Zhou S, Sawicki A, Willows RD, Luo M. FEBS Lett 586 205-210 (2012)
  8. Chaperone role for proteins p618 and p892 in the extracellular tail development of Acidianus two-tailed virus. Scheele U, Erdmann S, Ungewickell EJ, Felisberto-Rodrigues C, Ortiz-Lombardía M, Garrett RA. J Virol 85 4812-4821 (2011)
  9. iTRAQ-based quantitative proteomics analysis of rice leaves infected by Rice stripe virus reveals several proteins involved in symptom formation. Wang B, Hajano JU, Ren Y, Lu C, Wang X. Virol J 12 99 (2015)
  10. Highly regulated, diversifying NTP-dependent biological conflict systems with implications for the emergence of multicellularity. Kaur G, Burroughs AM, Iyer LM, Aravind L. Elife 9 e52696 (2020)
  11. The Ycf54 protein is part of the membrane component of Mg-protoporphyrin IX monomethyl ester cyclase from barley (Hordeum vulgare L.). Bollivar D, Braumann I, Berendt K, Gough SP, Hansson M. FEBS J 281 2377-2386 (2014)
  12. BchJ and BchM interact in a 1 : 1 ratio with the magnesium chelatase BchH subunit of Rhodobacter capsulatus. Sawicki A, Willows RD. FEBS J 277 4709-4721 (2010)
  13. Phosphorylation of GENOMES UNCOUPLED 4 Alters Stimulation of Mg Chelatase Activity in Angiosperms. Richter AS, Hochheuser C, Fufezan C, Heinze L, Kuhnert F, Grimm B. Plant Physiol 172 1578-1595 (2016)
  14. Abolition of magnesium chelatase activity by the gun5 mutation and reversal by Gun4. Davison PA, Hunter CN. FEBS Lett 585 183-186 (2011)
  15. Structure of the cyanobacterial Magnesium Chelatase H subunit determined by single particle reconstruction and small-angle X-ray scattering. Qian P, Marklew CJ, Viney J, Davison PA, Brindley AA, Söderberg C, Al-Karadaghi S, Bullough PA, Grossmann JG, Hunter CN. J Biol Chem 287 4946-4956 (2012)
  16. A structural analysis of the AAA+ domains in Saccharomyces cerevisiae cytoplasmic dynein. Gleave ES, Schmidt H, Carter AP. J Struct Biol 186 367-375 (2014)
  17. The allosteric role of the AAA+ domain of ChlD protein from the magnesium chelatase of synechocystis species PCC 6803. Adams NB, Reid JD. J Biol Chem 288 28727-28732 (2013)
  18. Structural and functional consequences of removing the N-terminal domain from the magnesium chelatase ChlH subunit of Thermosynechococcus elongatus. Adams NB, Marklew CJ, Qian P, Brindley AA, Davison PA, Bullough PA, Hunter CN. Biochem J 464 315-322 (2014)
  19. Structural insights into the catalytic mechanism of Synechocystis magnesium protoporphyrin IX O-methyltransferase (ChlM). Chen X, Wang X, Feng J, Chen Y, Fang Y, Zhao S, Zhao A, Zhang M, Liu L. J Biol Chem 289 25690-25698 (2014)
  20. A BchD (magnesium chelatase) mutant of rhodobacter sphaeroides synthesizes zinc bacteriochlorophyll through novel zinc-containing intermediates. Jaschke PR, Hardjasa A, Digby EL, Hunter CN, Beatty JT. J Biol Chem 286 20313-20322 (2011)
  21. Letter The catalytic power of magnesium chelatase: a benchmark for the AAA(+) ATPases. Adams NB, Brindley AA, Hunter CN, Reid JD. FEBS Lett 590 1687-1693 (2016)
  22. Characterization of the magnesium chelatase from Thermosynechococcus elongatus. Adams NB, Marklew CJ, Brindley AA, Hunter CN, Reid JD. Biochem J 457 163-170 (2014)
  23. Reduced chlorophyll biosynthesis in heterozygous barley magnesium chelatase mutants. Braumann I, Stein N, Hansson M. Plant Physiol Biochem 78 10-14 (2014)
  24. Catalytic turnover triggers exchange of subunits of the magnesium chelatase AAA+ motor unit. Lundqvist J, Braumann I, Kurowska M, Müller AH, Hansson M. J Biol Chem 288 24012-24019 (2013)
  25. Nanomechanical and Thermophoretic Analyses of the Nucleotide-Dependent Interactions between the AAA(+) Subunits of Magnesium Chelatase. Adams NB, Vasilev C, Brindley AA, Hunter CN. J Am Chem Soc 138 6591-6597 (2016)
  26. FERROCHELATASE: THE CONVERGENCE OF THE PORPHYRIN BIOSYNTHESIS AND IRON TRANSPORT PATHWAYS. Hunter GA, Al-Karadaghi S, Ferreira GC. J Porphyr Phthalocyanines 15 350-356 (2011)
  27. The uroS and yifB Genes Conserved among Tetrapyrrole Synthesizing-Deficient Bacteroidales Are Involved in Bacteroides fragilis Heme Assimilation and Survival in Experimental Intra-abdominal Infection and Intestinal Colonization. Parker AC, Bergonia HA, Seals NL, Baccanale CL, Rocha ER. Infect Immun 88 e00103-20 (2020)
  28. Inducing the oxidative stress response in Escherichia coli improves the quality of a recombinant protein: magnesium chelatase ChlH. Müller AH, Sawicki A, Zhou S, Tabrizi ST, Luo M, Hansson M, Willows RD. Protein Expr Purif 101 61-67 (2014)
  29. Barley Viridis-k links an evolutionarily conserved C-type ferredoxin to chlorophyll biosynthesis. Stuart D, Sandström M, Youssef HM, Zakhrabekova S, Jensen PE, Bollivar D, Hansson M. Plant Cell 33 2834-2849 (2021)
  30. Impact of Porphyrin Binding to GENOMES UNCOUPLED 4 on Tetrapyrrole Biosynthesis in planta. Fölsche V, Großmann C, Richter AS. Front Plant Sci 13 850504 (2022)
  31. Conformational variability of cyanobacterial ChlI, the AAA+ motor of magnesium chelatase involved in chlorophyll biosynthesis. Shvarev D, Scholz AI, Moeller A. mBio 14 e0189323 (2023)
  32. Heterologous Expression of the Barley (Hordeum vulgare L.) Xantha-f, -g and -h Genes that Encode Magnesium Chelatase Subunits. Mahdi R, Stuart D, Hansson M, Youssef HM. Protein J 39 554-562 (2020)
  33. Photosynthetic characteristics and genetic mapping of a new yellow leaf mutant crm1 in Brassica napus. Zhang H, Zhang W, Xiang F, Zhang Z, Guo Y, Chen T, Duan F, Zhou Q, Li X, Fang M, Li X, Li B, Zhao X. Mol Breed 43 80 (2023)
  34. Comment Putting metal in the middle. Bollivar DW. Structure 18 277-278 (2010)


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