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Enhancing photosynthesis by synthetic biology and adaptive evolution

 ERC Synergy Grant project PhotoRedesign

1200px-European_Research_Council_logo.svgphotoredesign

Only a fraction of the solar spectrum is used by the light reactions and high light intensities can impair and even damage the process. In consequence, expanding the solar spectrum and making the process more stress tolerant could have a strong impact on the production of food, energy or high value compounds. However, the photosynthetic machinery is one of the most complex systems in nature and thus has so far largely resisted man-made improvements by conventional approaches. Therefore, there is an urgent need to develop novel concepts to redesign their light-harvesting and photochemical capacity, as well as to establish new model systems and toolkits for the next generation of photosynthesis researchers. The overall objective of PhotoRedesign is to design in the model organism Synechocystis light reactions that can harvest and safely convert energy from an expanded solar spectrum. To this end, photosystems from different photoautotrophic model organisms – the purple bacterium Rhodobacter sphaeroides, the cyanobacterium Synechocystis PCC6803 and the flowering plant Arabidopsis thaliana - will be combined by synthetic biology, together with their native or de novo-designed antennas, and the capacity of the reimagined organism to cope with enhanced light harvesting will be enhanced by adaptive laboratory evolution.

Participants:

Dario Leister (Munich)

Neil Hunter (Sheffield)

Josef Komenda (Czech Academy)

 

Publications:

2022

  • Bečková M, Sobotka R, Komenda J (2022) Photosystem II antenna modules CP43 and CP47 do not form a stable ‘no reaction centre complex’ in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res https://link.springer.com/article/10.1007/s11120-022-00896-w
  • Rahimzadeh-Karvansara P, Pascual-Aznar G, Bečková M, Komenda J (2022) Psb34 protein modulates binding of high-light-inducible proteins to CP47-containing photosystem II assembly intermediates in the cyanobacterium Synechocystis sp. PCC 6803. Photosynth Res https://doi.org/10.1007/s11120-022-00908-9
  • Knoppová J, Sobotka R, Yu J, Bečková M, Pilný J, Trinugroho JP, Csefalvay L, B00904ína D, Nixon PJ, Komenda J (2022) Assembly of D1/D2 complexes of photosystem II: Binding of pigments and a network of auxiliary proteins. Plant Physiol 189: 790-804
  • Konert M, Wysocka A, Koník P, Sobotka R (2022) High-light-inducible proteins HliA and liB: pigment binding and protein-protein interactions. Photosynth Res https://doi.org/10.1007/s11120-022-00904-z
  • MacGregor-Chatwin C, Nürnberg DJ, Jackson PJ, Vasilev C, Hitchcock A, Ho MY, Shen G, Gisriel CJ, Wood WHJ, Mahbub M. Selinger VM, Johnson MP, Dickman MJ, Rutherford AW, Bryant DA,  Hunter CN (2022) Changes in supramolecular organization of cyanobacterial thylakoid membrane complexes in response to far-red light photoacclimation. Sci Adv 8: eabj4437
  • Qian P, Gardiner AT, Šímová I, Naydenova K, Croll TI, Jackson PJ, Nupur, Kloz M, Čubáková P, Kuzma M, Zeng Y, Castro-Hartmann P, van Knippenberg B, Goldie KN, Kaftan D, Hrouzek P, Hájek J, Agirre J, Siebert CA, Bína D, Sader K, Stahlberg H, Sobotka R, Russo CJ, Polívka T, Hunter CN, Koblížek M (2022) 2.4 Å structure of the double-ring Gemmatimonas phototrophica photosystem. Sci Adv 8: abk3139
  • Vasilev C, Swainsbury DJK, Cartron ML, Martin EC, Kumar S, Hobbs JK, Johnson MP, Hitchcock A, Hunter CN (2022) FRET measurement of cytochrome bc1 and reaction centre complex proximity in live Rhodobacter sphaeroides cells. Biochim Biophys Acta 1863: 148508

2021

  • Hitchcock A, Hunter CN, Sobotka R, Komenda J, Dann M, Leister D (2021) Redesigning the photosynthetic light reactions to enhance photosynthesis – the PhotoRedesign consortium. Plant J 109: 23-34
  • Dann M, Ortiz EM, Thomas M, Guljamow A, Lehmann M, Schäfer H, Leister D (2021) Enhancing photosynthesis at high light levels by adaptive laboratory evolution. Nat Plants 7: 681-695
  • Knoppova J, Yu J, Janouskovec J, Halada P, Nixon PJ, Whitelegge JP, Komenda J (2021) The Photosystem II Assembly Factor Ycf48 from the Cyanobacterium Synechocystis sp. PCC 6803 Is Lipidated Using an Atypical Lipobox Sequence. Int J Mol Sci 22: 3733
  • Chen GE, Hitchcock A, Mares J, Sobotka R (2021) Evolution of Ycf54-independent chlorophyll biosynthesis in cyanobacteria PNAS 118: e2024633118
  • Pacual-Aznar G, Konert G, Beckova M, Kotabova E, Gardian Z, Knoppova J, Bucinska L, Kana R, Sobotka R, Komenda J (2021) Psb35 Protein Stabilizes the CP47 Assembly Module and Associated High-Light Inducible Proteins during the Biogenesis of Photosystem II in the Cyanobacterium Synechocystis sp. PCC6803. Plant Cell Phys 62: 178-190
  • Canonico M, Konert G, Crepin A, Sediva B, Kana R (2021) Gradual Response of Cyanobacterial Thylakoids to Acute High-Light Stress—Importance of Carotenoid Accumulation. Cells 10: 1916
  • Chiu YF, Fu HY, Skotnicová P, Lin KM, Komenda J, Chu HA (2021) Tandem gene amplification restores photosystem II accumulation in cytochrome b559 mutants of cyanobacteria. New Phytol 223: 766-780
  • Lehmann M, Vamvak E, Torrado A, Jahns P, Dann M, Rosenhammer L, Aziba A, Leister D, Rühle T (2021) Introduction of the Carotenoid Biosynthesis α-Branch Into Synechocystis sp. PCC 6803 for Lutein Production. Front Plant Sci https://doi.org/10.3389/fpls.2021.699424
  • Skotnicová P, Staleva-Musto H, Kuznetsova V, Bina D, Konert MM, Lu S, Polivka T, Sobotka R (2021) Plant LHC-like proteins show robust folding and static non-photochemical quenching. Nat Commun 12: 6890
  • Chen GE, Adams NBP, Jackson PJ, Dickman MJ, Hunter, CN (2021) How the O2-dependent Mg-protoporphyrin monomethyl ester cyclase forms the fifth ring of chlorophylls. Nature Plants 7: 365-375
  • Gardiner AT, Naydenova K, Castro-Hartmann P, Nguyen-Phan T C, Russo CJ, Sader K, Hunter CN, Cogdell RJ, Qian P (2021) The 2.4 Å cryo-EM structure of a heptameric light-harvesting 2 complex reveals two carotenoid energy transfer pathways. Sci Adv 7: abe4650
  • Qian P, Swainsbury DJK, Croll TI, Salisbury JH, Martin EC, Jackson PJ, Hitchcock A, Castro-Hartmann P, Sader K,  Hunter CN (2021) Cryo-EM structure of the Rhodobacter sphaeroides RC-LH1 core monomer complex at 2.5 Å. Biochem J 478: 3775-3790
  • Sener M, Levy S, Stone JE, Christensen AJ, Isralewitz B, Patterson R, Borkiewicz K, Carpenter J, Hunter CN, Luthey-Schulten Z, Cox D (2021) Multiscale modeling and cinematic visualization of photosynthetic energy conversion processes from electronic to cell scales. Parallel Comp 102: 102698
  • Qian P, Croll TI, Swainsbury DJK, Castro-Hartmann P, Moriarty NW, Sader K, Hunter CN (2021) Cryo-EM structure of the Rhodospirillum rubrum RC-LH1 complex at 2.5 Å. Biochem J 478:3253-3263
  • Qian P, Swainsbury DJK, Croll TI, Salisbury JH, Martin EC, Jackson PJ, Hitchcock A, Castro-Hartmann P, Sader K, Hunter C (2021) Cryo-EM structure of the Rhodobacter sphaeroides RC-LH1 core dimer complex at 2.9 Å. Biochem J 478: 3923-3937
  • Swainsbury DJK, Qian P, Jackson PJ, Faries KM, Niedzwiedzki D, Martin EC, Farmer DA, Malone LA, Thompson RF, Ranson NA, Canniffe DP, Dickman MJ, Holten D, Kirmaier C, Hitchcock, A Hunter CN (2021) Structures of Rhodopseudomonas palustris RC-LH1 complexes with open or closed quinone channels. Sci Adv 7: abe2631
  • Flannery SE, Pastorelli F, Wood WHJ, Hunter CN, Dickman MJ, Jackson PJ, Johnson MP (2021) Comparative proteomics of thylakoids from Arabidopsis grown in laboratory and field conditions. Plant Direct 5: e355
  • Qian P, Swainsbury DJK, Croll TI, Castro-Hartmann P, Divitini G, Sader K, Hunter CN (2021) Cryo-EM Structure of the Rhodobacter sphaeroides Light-Harvesting 2 Complex at 2.1 Å. Biochem 60: 3302-3314

2020

  • Sutherland GA, Polak D, Swainsbury DJK, Wang S, Spano FC, Auman DB, Bossanyi DG, Pidgeon JP, Hitchcock A, Musser J, Anthony JE, Dutton L, Clark J, Hunter CN (2020) A Thermostable Protein Matrix for Spectroscopic Analysis of Organic Semiconductors. J Am Chem Soc 142: 13898-13907
  • Huang X, Hunter N, Vasilev C (2020) Multicomponent Nanoscale Patterning of Functional Light-Harvesting Protein Complexes by Local Oxidation Lithography. Adv Mat 8: 2001670
  • Proctor MS, Pazdernik M, Jackson PJ, Pilny J, Martin EC, Dickman MJ, Canniffe DP, Johnson MP, Hunter CN, Sobotka R, Hitchcock A (2020) Xanthophyll carotenoids stabilise the association of cyanobacterial chlorophyll synthase with the LHC-like protein HliD. Biochem J 477: 4021-4036
  • Radek K, Steinbach G, Sobotka R, Vamosi G, Komenda J (2020) Fast Diffusion of the Unassembled PetC1-GFP Protein in the Cyanobacterial Thylakoid Membrane. Life 11: 15
  • Adams NBP, Bisson C, Brindley AA et al (2020) The active site of magnesium chelatase. Nat Plants 6: 1491-1502
  • Leister D (2020) Alternative electron pathways in photosynthesis: strength in numbers. New Phytol 228: 1166-1168
  • Chen GE, Hunter CN (2020) Protochlorophyllide synthesis by recombinant cyclases from eukaryotic oxygenic phototrophs and the dependence on Ycf54. Biochem J 477: 2313-2325