The goal of this project is to understand how plants can oxidize water to molecular oxygen, electrons and protons. Plants, green algae and cyanobacteria are unique in that they can use the energy in sun- light to oxidize water. This reaction occurs at a multi protein complex, photosystem II, in the chloroplast and is tightly regulated. If we can fully understand the mechanism of water oxidation and its regulation, we can use that knowledge to create artificial pho- tosynthetic devices to produce clean and renewable energy.

Samuelsson Goran 1150Plants produce oxygen that is released to the atmosphere. Oxygen is important for most living organisms.
Photosystem II (PSII) uses sunlight to split water, an ener- getically unfavourable reaction in which electrons and protons are extracted from water and oxygen is released as a by-product. Understanding this process is crucial for the future development of clean, renewable and unlimited energy sources.

slim 2 slim 1
Post doc from New Zealand at the lab bench. Kits used in molecular biology.

slim 3We have been focusing on the role of two lumenal proteins in the water oxidation process,PsbO and Cah3,which are associated with the thylakoid membrane.We have known for many years how electrons are transported in the photosynthetic light reac- tions,but we have very limited information on how the protons are transported. Protons must be transported away from the catalytic centre, otherwise the oxidation reaction cannot occur with full efficiency. If water oxidation is hampered, then donor side photoinhibition occurs and the whole photosynthetic machinery will be destroyed.Therefore, one of my tasks is to describe how protons,released in the water oxidation process,are transported away from the catalytic centre and into the lumen. We have recently presented convincing evidence supporting the hypothesis that bicarbonate acts as a proton acceptor in the water-splitting process in PSII. Lumenal carbonic anhydrase, Cah3, identified by us, supplies bicarbonate required for this function.This was shown in one of our photosynthetic model organisms, Chlamydomonas reinhardtii.

Another important constituent of the water-oxidizing complex is the PsbO protein.This protein is conserved in all oxygen-producing organisms and has been studied for at least 20 years, but its function is still unknown.We believe that its role, in addition to stabilizing the Mn4Ca cluster in photosystem II,is to regulate transport of substrate-water to the catalytic centre and and to transport product-protons away from the water oxidation site.The PsbO protein undergoes a pH-dependent conformational change that in turn has influence on its capacity to bind calcium and manganese.We propose that light-induced structural dynamics of the PsbO is of functional relevance for the regulation of proton release and for forming a proton-sensing proton transport pathway.The activities of both proteins may be redox-regulated through their S-S bridges.
sweden_greySvensk sammanfattning...

Publications list

  1. Vyacheslav (Slava) Klimov (1945-2017): A scientist par excellence, a great human being, a friend, and a Renaissance man
    Photosynth Res. 2018, 136(1):1-16
  2. Crystal Structure and Functional Characterization of Photosystem II-Associated Carbonic Anhydrase CAH3 in Chlamydomonas reinhardtii
    Plant Physiol. 2015, 167(3):950-62
  3. Mobile hydrogen carbonate acts as proton acceptor in photosynthetic water oxidation
    PNAS 2014, 111(17):6299-6304
  4. Efficiency of photosynthetic water oxidation at ambient and depleted levels of inorganic carbon
    Photosynth Res. 2013; 117(1-3):401-12
  5. Burén S, Ortega-Villasante C, Otvös K, Samuelsson G, Bakó L, Villarejo A
    Use of the Foot-and-Mouth Disease Virus 2A Peptide Co-Expression System to Study Intracellular Protein Trafficking in Arabidopsis
    PLoS One 2012;7(12):e51973
  6. Huang S, Hainzl T, Grundström C, Forsman C, Samuelsson G, Sauer-Eriksson AE
    Structural Studies of β-Carbonic Anhydrase from the Green Alga Coccomyxa: Inhibitor Complexes with Anions and Acetazolamide
    PLoS One. 2011;6(12):e28458. Epub 2011 Dec 5.
  7. Shitov AV, Zharmukhamedov SK, Shutova TV, Allakhverdiev SI, Samuelsson G, Klimov VV
    A carbonic anhydrase inhibitor induces bicarbonate-reversible suppression of electron transfer in pea photosystem 2 membrane fragments
    Journal of Photochemistry and Photobiology B: Biology: 2011 104:366-371
  8. Burén S, Ortega-Villasante C, Blanco-Rivero A, Martinez-Bernardini A, Shutova T, Shevela D, Messinger J, Bako L, Villarejo A, Samuelsson G
    Importance of Post-Translational Modifications for Functionality of a Chloroplast-Localized Carbonic Anhydrase (CAH1) in Arabidopsis thaliana
    PLoS one: 2011 6:e21021
  9. Aksmann A, Shutova T, Samuelsson G, Tukaj Z
    The mechanism of anthracene interaction with photosynthetic apparatus: A study using intact cells, thylakoid membranes and PS II complexes isolated from Chlamydomonas reinhardtii
    Aquatic Toxicology: 2011 104:205-210
  10. Renberg L, Johansson AI, Shutova T, Stenlund H, Aksmann A, Raven JA, Gardeström P, Moritz T, Samuelsson G
    A metabolomic approach to study major metabolite changes during acclimation to limiting CO2 in Chlamydomonas reinhardtii
    Plant Physiology: 2010 154:187-196
  11. Nikitina J, Shutova T, Melnik B, Chernyshov S, Marchenkov V, Semisotnov G, Klimov V, Samuelsson G
    Importance of a single disulfide bond for the PsbO protein of photosystem II: protein structure stability and soluble overexpression in Escherichia coli

    Photosynthesis Research: 2008 98:391-403
  12. Shutova T, Kenneweg H, Buchta J, Nikitina J, Terentyev V, Chernyshov S, Andersson B, Allakhverdiev SI, Klimov VV, Dau H, Junge W, Samuelsson G
    The photosystem II-associated Cah3 in Chlamydomonas enhances the O2 evolution rate by proton removal
    The EMBO Journal: 2008 27:782-791
  13. Kupriyanova E, Villarejo A, Markelova A, Gerasimenko L, Zavarzin G, Samuelsson G, Los DA, Pronina N
    Extracellular carbonic anhydrase of the stromatolite-forming cyanobacterium Microcoleus chthonoplastes
    Microbiology: 2007 153:1149-1156
  14. Lundin B, Thuswaldner S, Shutova T, Eshaghi S, Samuelsson G, Barber J, Andersson B, Spetea C
    Subsequent events to GTP binding by the plant PsbO protein: Structural changes, GTP hydrolysis and dissociation from the photosystem II complex.
    Biochimica et Biophysica Acta: 2007 1767:500-508
  15. Shutova T, Klimov VV, Andersson B, Samuelsson G
    A cluster of carboxylic groups in PsbO protein is involved in proton transfer from the water oxidizing complex of Photosystem II
    Biochimica et Biophysica Acta: 2007 1767:434-440
  16. Villarejo A, Buren S, Larsson S, Dejardin A, Monne M, Rudhe C, Karlsson J, Jansson S, Lerouge P, Rollands N, von Heijne G, Grebe M, Bako L, Samuelsson G
    Evidence for a protein transported through the secretory pathway en route to the higher plant chloroplast
    Nature Cell Biology: 2005 7:1224-1231
  17. Rouhier N, Villarejo A, Srivastava M, Gelhaye E, Keech O, Droux M, Finkemeier I, Samuelsson G, Dietz KJ, Jacquot J-P, Wingsle G
    Identification of plant glutaredoxin targets
    Antioxid Redox Signal: 2005 7:919-929
  18. Shutova T, Nikitina J, Deikus G, Andersson B, Klimov V, Samuelsson G
    Structural dynamics of the manganese-stabilizing protein - Effect of pH, calcium, and manganese
    Biochemistry: 2005 44:15182-15192
  19. Moskvin OV, Shutova TV, Khristin MS, Ignatova LK, Villarejo A, Samuelsson G, Klimov VV, Ivanov BN
    Carbonic anhydrase activities in pea thylakoids
    Photosynth Res: 2004 79:93-100
  20. Shutova T, Villarejo A, Zietz B, Klimov V, Gillbro T, Samuelsson G, Renger G
    Comparative studies on the properties of the extrinsic manganese-stabilizing protein from higher plants and of a synthetic peptide of its C-terminus
    Biochimica Et Biophysica Acta-Bioenergetics: 2003 1604:95-104
  21. Hanson DT, Franklin LA, Samuelsson G, Badger MR
    The Chlamydomonas reinhardtii cia3 mutant lacking a thylakoid lumen-localized carbonic anhydrase is limited by CO2 supply to rubisco and not photosystem II function in vivo
    Plant Physiol: 2003 132:2267-2275
  22. Villarejo A, Shutova T, Moskvin O, ForssEn M, Klimov VV, Samuelsson G
    A photosystem II-associated carbonic anhydrase regulates the efficiency of photosynthetic oxygen evolution
    EMBO J: 2002 21:1930-1938
  23. Moroney JV, Bartlett SG, Samuelsson G
    Carbonic anhydrases in plants and algae
    Plant Cell and Environment: 2001 24:141-153
  24. Rojdestvenski I, Park YI, Karlsson J, Oquist G, Samuelsson G
    A carbonic anhydrase catalyzed CO2 pump in Chlamydomonas reinhardtii: In vivo experiments, computer modelling, and theory
    Russian Journal of Plant Physiology: 2000 47:613-621
  25. Siedlecka A, Gardestrom P, Samuelsson G, Kleczkowski LA, Krupa Z
    A relationship between carbonic anhydrase and rubisco in response to moderate cadmium stress during light activation of photosynthesis
    Zeitschrift Fur Naturforschung C-a Journal of Biosciences: 1999 54:759-763
  26. Park YI, Karlsson J, Rojdestvenski I, Pronina N, Klimov V, Oquist G, Samuelsson G
    Role of a novel photosystem II-associated carbonic anhydrase in photosynthetic carbon assimilation in Chlamydomonas reinhardtii
    FEBS Lett: 1999 444:102-105
  27. Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV, Samuelsson G
    A novel alpha-type carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2
    EMBO J: 1998 17:1208-1216
  28. Eriksson M, Villand P, Gardestrom P, Samuelsson G
    Induction and regulation of expression of a low-CO2-induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii
    Plant Physiology: 1998 116:637-641
  29. Hiltonen T, Bjorkbacka H, Forsman C, Clarke AK, Samuelsson G
    Intracellular beta-carbonic anhydrase of the unicellular green alga Coccomyxa
    Plant Physiology: 1998 117:1341-1349
  30. Villand P, Eriksson M, Samuelsson G
    Carbon dioxide and light regulation of promoters controlling the expression of mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii
    Biochem J: 1997 327:51-57
  31. Karlsson J, Spear E, Mason CB, Moroney JV, Samuelsson G, Husic HD
    Carbonic anhydrase is associated with the thylakoid membrane in Chlamydomonas reinhardtii
    Plant Physiology: 1997 114:1086-1086
  32. Larsson S, Bjorkbacka H, Forsman C, Samuelsson G, Olsson O
    Molecular cloning and biochemical characterization of carbonic anhydrase from Populus tremula x tremuloides
    Plant Molecular Biology: 1997 34:583-592
  33. Palmqvist K, delosRios A, Ascaso C, Samuelsson G
    Photosynthetic carbon acquisition in the lichen photobionts Caccomyxa and Trebouxia (Chlorophyta)
    Physiologia Plantarum: 1997 101:67-76
  34. Siedlecka A, Krupa Z, Samuelsson G, Oquist G, Gardestrom P
    Primary carbon metabolism in Phaseolus vulgaris plants under Cd/Fe interaction
    Plant Physiology and Biochemistry: 1997 35:951-957
  35. Villand P, Eriksson M, Samuelsson G
    Regulation of genes by the environmental CO2-level in
    Plant Physiology: 1997 114:1334-1334
  36. Hiltonen T, Clarke AK, Karlsson J, Samuelsson G
    A cDNA coding for glutathione S-transferase from the unicellular green algae Coccomyxa sp
    Gene: 1996 176:263-264
  37. Eriksson M, Karlsson J, Ramazanov Z, Gardestrom P, Samuelsson G
    Discovery of an algal mitochondrial carbonic anhydrase: Molecular cloning and characterization of a low-CO2-induced polypeptide in Chlamydomonas reinhardtii
    Proceedings of the National Academy of Sciences of the United States of America: 1996 93:12031-12034
  38. Kromer S, Gardestrom P, Samuelsson G
    Regulation of the supply of cytosolic oxaloacetate for mitochondrial metabolism via phospho enolpyruvate carboxylase in barley leaf protoplasts .1. The effect of covalent modification on PEPC activity, pH response, and kinetic properties
    Biochimica Et Biophysica Acta-General Subjects: 1996 1289:343-350
  39. Kromer S, Gardestrom P, Samuelsson G
    Regulation of the supply of oxaloacetate for mitochondrial metabolism via phospho enolpyruvate carboxylase in barley leaf protoplasts .2. Effects of metabolites on PEPC activity at different activation states of the protein
    Biochimica Et Biophysica Acta-General Subjects: 1996 1289:351-361
  40. Karlsson J, Hiltonen T, Husic HD, Ramazanov Z, Samuelsson G
    Intracellular Carbonic-Anhydrase of Chlamydomonas-Reinhardtii
    Plant Physiology: 1995 109:533-539
  41. Eriksson M, Gardestrom P, Samuelsson G
    Isolation, Purification, and Characterization of Mitochondria from Chlamydomonas-Reinhardtii
    Plant Physiology: 1995 107:479-483
  42. Hiltonen T, Karlsson J, Palmqvist K, Clarke AK, Samuelsson G
    Purification and Characterization of an Intracellular Carbonic-Anhydrase from the Unicellular Green-Alga Coccomyxa
    Planta: 1995 195:345-351
  43. Karlsson J, Ramazanov Z, Hiltonen T, Gardestrom P, Samuelsson G
    Effect of Vanadate on Photosynthesis and the Atp Adp Ratio in Low-Co2-Adapted Chlamydomonas-Reinhardtii Cells
    Planta: 1994 192:46-51
  44. Palmqvist K, Samuelsson G, Badger MR
    Photobiont-Related Differences in Carbon Acquisition among Green-Algal Lichens
    Planta: 1994 195:70-79
  45. Hofslagare O, Sjoberg S, Samuelsson G
    The Effect of Arsenate and Arsenite on Photosynthesis in Scenedesmus-Obliquus - a Potentiometric Study in a Closed Co2-System
    Chemical Speciation and Bioavailability: 1994 6:95-102
  46. Borodin V, Gardestrom P, Samuelsson G
    The Effect of Light Quality on the Induction of Efficient Photosynthesis under Low Co2 Conditions in Chlamydomonas-Reinhardtii and Chlorella-Pyrenoidosa
    Physiologia Plantarum: 1994 92:254-260
  47. Pawlik B, Skowronski T, Ramazanow Z, Gardestrom P, Samuelsson G
    Ph-Dependent Cadmium Transport Inhibits Photosynthesis in the Cyanobacterium Synechocystis-Aquatilis
    Environmental and Experimental Botany: 1993 33:331-337
  48. Falk S, Leverenz JW, Samuelsson G, Oquist G
    Changes in Photosystem-Ii Fluorescence in Chlamydomonas-Reinhardtii Exposed to Increasing Levels of Irradiance in Relationship to the Photosynthetic Response to Light
    Photosynthesis Research: 1992 31:31-40
  49. Falk S, Samuelsson G
    Recovery of Photosynthesis and Photosystem-Ii Fluorescence in Chlamydomonas-Reinhardtii after Exposure to 3 Levels of High Light
    Physiologia Plantarum: 1992 85:61-68
  50. Palmqvist K, Ramazanov ZM, Samuelsson G
    Role of Carbonic-Anhydrase in Assimilation of Inorganic Carbon in Dunaliella-Salina
    Soviet Plant Physiology: 1991 38:339-345
  51. Palmqvist K, Sundblad LG, Wingsle G, Samuelsson G
    Acclimation of Photosynthetic Light Reactions During Induction of Inorganic Carbon Accumulation in the Green-Alga Chlamydomonas-Reinhardtii
    Plant Physiology: 1990 94:357-366
  52. Sundblad LG, Samuelsson G, Wigge B, Gardestrom P
    Luminescence Decay Kinetics in Relation to Quenching and Stimulation of Dark Fluorescence from High and Low Co2 Adapted Cells of Scenedesmus-Obliquus and Chlamydomonas-Reinhardtii
    Photosynthesis Research: 1990 23:269-282
  53. Palmqvist K, Ramazanov ZM, Gardestrom P, Samuelsson G
    Mechanisms of Adaptation of Microalgae to Conditions of Carbon-Dioxide Limitation of Photosynthesis - Possible Role of Carbonic-Anhydrase
    Soviet Plant Physiology: 1990 37:680-686
  54. Falk S, Samuelsson G, Oquist G
    Temperature-Dependent Photoinhibition and Recovery of Photosynthesis in the Green-Alga Chlamydomonas-Reinhardtii Acclimated to 12 and 27-Degrees-C
    Physiologia Plantarum: 1990 78:173-180
  55. Leverenz JW, Falk S, Pilstrom CM, Samuelsson G
    The Effects of Photoinhibition on the Photosynthetic Light-Response Curve of Green Plant-Cells (Chlamydomonas-Reinhardtii)
    Planta: 1990 182:161-168
  56. Palmqvist K, Ramazanov Z, Samuelsson G
    The Role of Extracellular Carbonic-Anhydrase for Accumulation of Inorganic Carbon in the Green-Alga Chlamydomonas-Reinhardtii - a Comparison between Wild-Type and Cell-Wall-Less Mutant-Cells
    Physiologia Plantarum: 1990 80:267-276